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In addition to its obligatory symbiont Buchnera aphidicola, the pea aphid Acyrthosiphon pisum can harbor several facultative bacterial symbionts which can be mutualistic in the context of various ecological interactions. Belonging to a genus where many members have been described as pathogen in invertebrates, Serratia symbiotica is one of the most common facultative partners found in aphids. The recent discovery of strains able to grow outside their host allowed us to simulate environmental acquisition of symbiotic bacteria by aphids. Here, we performed an experiment to characterize the A. pisum response to the ingestion of the free-living S. symbiotica CWBI-2.3T in comparison to the ingestion of the pathogenic Serratia marcescens Db11 at the early steps in the infection process. We found that, while S. marcescens Db11 killed the aphids within a few days, S. symbiotica CWBI-2.3T did not affect host survival and colonized the whole digestive tract within a few days. Gene expression analysis of immune genes suggests that S. symbiotica CWBI-2.3T did not trigger an immune reaction, while S. marcescens Db11 did, and supports the hypothesis of a fine-tuning of the host immune response set-up for fighting pathogens while maintaining mutualistic partners. Our results also suggest that the lysosomal system and the JNK pathway are possibly involved in the regulation of invasive bacteria in aphids and that the activation of the JNK pathway is IMD-independent in the pea aphid.

Developmental temperature plays important roles in the expression of insect traits through thermal developmental plasticity. We exposed the aphid parasitoid Aphidius colemani to different temperature regimes (10, 20, or 28 °C) throughout larval development and studied the expression of morphological and physiological traits indicator of fitness and heat tolerance in the adult. We showed that the mass decreased and the surface to volume ratio of parasitoids increased with the development temperature. Water content was not affected by rearing temperature, but parasitoids accumulated more lipids when reared at 20 °C. Egg content was not affected by developmental temperature, but adult survival was better for parasitoids reared at 20 °C. Finally, parasitoids developed at 20 °C showed the highest heat stupor threshold, whereas parasitoids developed at 28 °C showed the highest heat coma threshold (better heat tolerance CTmax1 and CTmax2, respectively), therefore only partly supporting the beneficial acclimation hypothesis. From a fundamental point of view, our study highlights the role of thermal plasticity (adaptive or not) on the expression of different life history traits in insects and the possible correlations that exist between these traits. From an applied perspective, these results are important in the context of biological control through mass release techniques of parasitoids in hot environments.

Brugia malayi is a human filarial nematode responsible for elephantiasis, a debilitating condition that is part of a broader spectrum of diseases called filariasis, including lymphatic filariasis and river blindness. Almost all filarial nematode species infecting humans live in mutualism with Wolbachia endosymbionts, present in somatic hypodermal tissues but also in the female germline which ensures their vertical transmission to the nematode progeny. These α-proteobacteria potentially provision their host with essential metabolites and protect the parasite against the vertebrate immune response. In the absence of Wolbachia wBm , B . malayi females become sterile, and the filarial nematode lifespan is greatly reduced. In order to better comprehend this symbiosis, we investigated the adaptation of wBm to the host nematode soma and germline, and we characterized these cellular environments to highlight their specificities. Dual RNAseq experiments were performed at the tissue-specific and ovarian developmental stage levels, reaching the resolution of the germline mitotic proliferation and meiotic differentiation stages. We found that most wBm genes, including putative effectors, are not differentially regulated between infected tissues. However, two wBm genes involved in stress responses are upregulated in the hypodermal chords compared to the germline, indicating that this somatic tissue represents a harsh environment to which wBm have adapted. A comparison of the B . malayi and C . elegans germline transcriptomes reveals a poor conservation of genes involved in the production of oocytes, with the filarial germline proliferative zone relying on a majority of genes absent from C . elegans . The first orthology map of the B . malayi genome presented here, together with tissue-specific expression enrichment analyses, indicate that the early steps of oogenesis are a developmental process involving genes specific to filarial nematodes, that likely result from evolutionary innovations supporting the filarial parasitic lifestyle.

Like many insects, aphids (Hemiptera: Aphididae) can host a wide diversity of symbiotic bacteria that can be important drivers of their evolutionary ecology. In addition to the nutritional obligate symbiont Buchnera aphidicola, these phloem-sap feeding insects can host various facultative symbionts whose functional diversity depends on complex interactions with the host genotype and environmental factors. During sampling in citrus orchards in northern Tunisia, we collected aphids on citrus plants. The specimens belonged either to the cotton-melon aphid Aphis gossypii or the green citrus aphid Aphis spiraecola. We analysed the prevalence of Arsenophonus, Serratia symbiotica, Hamiltonella defensa and Regiella insecticola, four facultative symbionts frequently found in the genus Aphis and potentially associated with phenotypic effects related to nutrition, protection against parasites and tolerance of high temperatures. We found that the diversity and prevalence of facultative symbionts differed between these two aphid species that exploit similar ecological niches. In particular, we found a high prevalence of Arsenophonus in A. gossypii populations and that the defensive symbiont H. defensa was only present in A. spiraecola populations. These results are discussed in light of the ecology and life cycles of each of the species of aphid studied.

Symbiotic bacteria are common in insects and can affect various aspects of their hosts’ biology. Although the effects of insect symbionts have been clarified for various insect symbiosis models, due to the difficulty of cultivating them in vitro , there is still limited knowledge available on the molecular features that drive symbiosis. Serratia symbiotica is one of the most common symbionts found in aphids. The recent findings of free-living strains that are considered as nascent partners of aphids provide the opportunity to examine the molecular mechanisms that a symbiont can deploy at the early stages of the symbiosis (i.e., symbiotic factors). In this work, a proteomic approach was used to establish a comprehensive proteome map of the free-living S. symbiotica strain CWBI-2.3 T . Most of the 720 proteins identified are related to housekeeping or primary metabolism. Of these, 76 were identified as candidate proteins possibly promoting host colonization. Our results provide strong evidence that S. symbiotica CWBI-2.3 T is well-armed for invading insect host tissues, and suggest that certain molecular features usually harbored by pathogenic bacteria are no longer present. This comprehensive proteome map provides a series of candidate genes for further studies to understand the molecular cross-talk between insects and symbiotic bacteria.

Endosymbiotic organisms are known to manipulate the reproductive biology of their hosts. Incomplete prevalence of endosymbiont inducing thelytokous parthenogenesis results in the coexistence of sexual and asexual individuals, and could account for the maintenance of sexual reproduction in certain populations or species. In the parasitoid Venturia canescens, arrhenotokous (\"sexual\") and thelytokous (\"asexual\") individuals occur sympatrically. We aimed to determine whether endosymbionts are implicated in the thelytoky of V. canescens. After screening females of the two reproductive modes for several reproductive parasites: bacteria (Wolbachia, Rickettsia, Bacteroidetes, Spiroplasma, Arsenophonus) and Microsporidia, we concluded that thelytoky in V. canescens is not induced by any of these parasites and confirmed its suitability as a biological model for solving the evolutionary enigma of the maintenance of sexual reproduction. [PUBLICATION ABSTRACT]

Many insects engage in symbiotic associations with diverse assemblages of bacterial symbionts that can deeply impact on their ecology and evolution. The intraspecific variation of symbionts remains poorly assessed while phenotypic effects and transmission behaviors, which are key processes for the persistence and evolution of symbioses, may differ widely depending on the symbiont strains. Serratia symbiotica is one of the most frequent symbiont species in aphids and a valuable model to assess this intraspecific variation since it includes both facultative and obligate symbiotic strains. Despite evidence that some facultative S. symbiotica strains exhibit a free-living capacity, the presence of these strains in wild aphid populations, as well as in insects with which they maintain regular contact, has never been demonstrated. Here, we examined the prevalence, diversity, and tissue tropism of S. symbiotica in wild aphids and associated ants. We found a high occurrence of S. symbiotica infection in ant populations, especially when having tended infected aphid colonies. We also found that the S. symbiotica diversity includes strains found located within the gut of aphids and ants. In the latter, this tissue tropism was found restricted to the proventriculus. Altogether, these findings highlight the extraordinary diversity and versatility of an insect symbiont and suggest the existence of novel routes for symbiont acquisition in insects.

Polyphagy is an adaptative strategy allowing species to develop and survive on multiple diets. Phytophagous insects can be exposed to sub-optimal resources, as host plants vary in nutritional quality. Some insects may rely on symbiotic bacteria to better utilize less favorable substrates. The invasive fruit fly Drosophila suzukii is a highly successful pest worldwide. The use of ripening and ripe fruits, a niche neglected by other drosophilids, and its polyphagy may have contributed to its global spread. The role of D. suzukii 's Wolbachia strain ( w Suz) remains unconfirmed, although a mutualistic role has been hypothesized via virus protection or dealing with abiotic stress. In some insect species, Wolbachia acts as a nutritional mutualist. This study explored the role of w Suz in D. suzukii adaptation to fluctuating diet regimes. To simulate a diet shift, we used Wolbachia -infected and uninfected flies, maintained on a corn-based (low-starch) or a grape-based (high-starch) diet for at least 10 generations. Then, we placed individuals from each line on one or the other diet for 30 days. The effects of Wolbachia and the diet treatments were assessed by quantifying female fecundity, egg-to-adult development time and survival, and offspring mass. The presence of Wolbachia positively affected female fecundity and offspring mass after a diet shift. Wolbachia also increased survival during larval development regardless of the diet, supporting its mutualistic role. Our results underline the role of w Suz on D. suzukii diet tolerance and performance. A better understanding of the role of symbionts in invasive species could help to improve management strategies.

1. Reaction norms depict the environmental effects on phenotypic traits and are used to predict the global change consequences on species distributions. However, studies performed at constant temperatures have limited ecological significance because expressed phenotypes depend on the range and frequency of environmental states. 2. Using Jensen's inequality (i.e. a mathematical property of nonlinear functions), we predicted that the effect of thermal fluctuations on the phenotype depends on the shape of the reaction norm. Thermal fluctuations around the optimal temperature are expected to reduce the phenotypic trait values, especially for specialists because of their narrower reaction norms. 3. This study measured the effects of diel fluctuations in developmental temperature on phenotypic expression of traits related to fitness and energetic resources in two strains of the parasitoid wasp Venturia canescens from different habitats: a thermal generalist strain and a specialist one. In a first experiment, we compared the effect of constant thermal regimes versus fluctuating ones having the same means (20, 25 and 30 °C) on reaction norms of life-history traits and of energetic reserves. In a second experiment, we examined the effects of a natural thermoperiod in the field on these traits. 4. Our results show that the shape of the reaction norm defines the phenotypic changes induced by the development under fluctuating thermal conditions. These results match the predictions of the Jensen's inequality. Moreover, our results emphasize the significance of taking into account several phenotypic life-history traits to study the adaptive value of phenotypic plasticity. We also show that the level of energetic resources depends on the mean developmental temperature and not on the thermal regime. Finally, the field experiment confirms that the phenotype of these parasitoids depends on the temperature variation. 5. Our study highlights the relevance of the Jensen's inequality to predict the effect of thermal fluctuations on fitness of parasitoids with contrasted thermal sensitivities.

Microorganism communities that live inside insects can play critical roles in host development, nutrition, immunity, physiology, and behavior. Over the past decade, high-throughput sequencing reveals the extraordinary microbial diversity associated with various insect species and provides information independent of our ability to culture these microbes. However, their cultivation in the laboratory remains crucial for a deep understanding of their physiology and the roles they play in host insects. Aphids are insects that received specific attention because of their ability to form symbiotic associations with a wide range of endosymbionts that are considered as the core microbiome of these sap-feeding insects. But, if the functional diversity of obligate and facultative endosymbionts has been extensively studied in aphids, the diversity of gut symbionts and other associated microorganisms received limited consideration. Herein, we present a culture-dependent method that allowed us to successfully isolate microorganisms from several aphid species. The isolated microorganisms were assigned to 24 bacterial genera from the Actinobacteria, Firmicutes, and Proteobacteria phyla and three fungal genera from the Ascomycota and Basidiomycota phyla. In our study, we succeeded in isolating already described bacteria found associated to aphids (e.g., the facultative symbiont Serratia symbiotica), as well as microorganisms that have never been described in aphids before. By unraveling a microbial community that so far has been ignored, our study expands our current knowledge on the microbial diversity associated with aphids and illustrates how fast and simple culture-dependent approaches can be applied to insects in order to capture their diverse microbiota members.