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International audience; Most insect herbivores are adapted to feed on a few host plants only, but the mechanisms underlying plant specialization are poorly understood. One of the dominant hypotheses is that insects inject an oral secretion into the plant that manipulates the plant's defences resulting in induced susceptibility. This hypothesis was tested on the pea aphid (Acyrthosiphon pisum), which forms multiple biotypes, each specialized on specific legume hosts. In particular, the hypothesis that a pea-adapted biotype can induce host susceptibility on pea and increase the fitness of a non-pea-adapted biotype was tested. Survival and fecundity of an alfalfa-adapted biotype on peas were enhanced by co-infestation but not by pre-infestation with a pea-adapted biotype. The electrical penetration graph (EPG) method was then used to dissect the components of the alfalfa biotype feeding behaviour on peas with and without co-infestation by the pea biotype. While probing time did not differ between these two conditions, differences were observed in most other EPG parameters. When co-infested with the pea-adapted biotype, the alfalfa-adapted biotype was more likely to establish a phloem feeding and exhibited a longer ingestion time on peas. Our results indicated that the pea-adapted biotype induced pea susceptibility by increasing the accessibility of non-pea-adapted aphids to the host phloem sap. As a result, the alfalfa biotype increased its survival and fecundity. These results contribute to understanding how aphids manipulate their specific host plants.

International audience; Due to their ability to parasitize various insect species, generalist parasitoids are widely used as biological control agents. They can be mass-reared and released in agroecosystems to control several pest species in various crops. However, the existence of genetic differentiation among populations of generalist parasitoid species is increasingly recognized and this can be associated with an adaptation to local conditions or to a reduced range of host species. Moreover, constraints of mass-rearing conditions can alter genetic variation within parasitoid populations released. These features could be associated with a reduced efficiency of the control of targeted pest species. Here, we focused on strawberry greenhouses where the control of aphids with the generalist parasitoid Aphidius ervi appears to be inefficient. We investigated whether this inefficiency may have both genetic and ecological bases comparing wild and commercial populations of A . ervi . We used two complementary genetic approaches: one based on the mitochondrial marker COI and one based on microsatellite markers. COI analysis showed a genetic differentiation within the A . ervi species, but the structure was neither associated with the commercial/wild status nor with host species factors. On the other hand, using microsatellite markers, we showed a genetic differentiation between commercial and wild A . ervi populations associated with a loss of genetic diversity within the mass-reared populations. Our ecological genetics study may potentially explain the weak efficiency of biological control of aphids in protected strawberry crops and enable to provide some insights to improve biological control.

International audience; In the last decade, the influence of microbial symbionts on ecological and physiological traits of their hosts has been increasingly recognized. However, most of these effects have been revealed under laboratory conditions, which oversimplifies the complexity of the factors involved in the dynamics of symbiotic associations in nature. The pea aphid, Acyrthosiphon pisum , forms a complex of plant-adapted biotypes, which strongly differ in the prevalence of their facultative endosymbionts. Some of the facultative endosymbionts of A. pisum have been shown to confer protection against natural enemies, among which Hamiltonella defensa is known to protect its host from parasitoid wasps. Here, we tested under natural conditions whether the endosymbiont communities of different A. pisum biotypes had a protective effect on their hosts and whether endosymbiotic associations and parasitoid communities associated with the pea aphid complex were linked. A space-time monitoring of symbiotic associations, parasitoid pressure and parasitoid communities was carried out in three A. pisum biotypes respectively specialized on Medicago sativa (alfalfa), Pisum sativum (pea), and Trifolium sp. (clover) throughout the whole cropping season. While symbiotic associations, and to a lesser extent, parasitoid communities were stable over time and structured mainly by the A. pisum biotypes, the parasitoid pressure strongly varied during the season and differed among the three biotypes. This suggests a limited influence of parasitoid pressure on the dynamics of facultative endosymbionts at a seasonal scale. However, we found a positive correlation between the α and β diversities of the endosymbiont and parasitoid communities, indicating interactions between these two guilds. Also, we revealed a negative correlation between the prevalence of H. defensa and Fukatsuia symbiotica in co-infection and the intensity of parasitoid pressure in the alfalfa biotype, confirming in field conditions the protective effect of this symbiotic combination.

Aphids use an alarm pheromone, E-&beta, farnesene (EBF), to warn conspecifics of potential danger. The antennal sensitivity and behavioural escape responses to EBF can be influenced by different factors. In the pea aphid, Acyrthosiphon pisum, different biotypes are adapted to different legume species, and within each biotype, different genotypes exist, which can carry or not Hamiltonella defensa, a bacterial symbiont that can confer protection against natural enemies. We investigate here the influence of the aphid genotype and symbiotic status on the escape behaviour using a four-way olfactometer and antennal sensitivity for EBF using electroantennograms (EAGs). Whereas the investigated three genotypes from two biotypes showed significantly different escape and locomotor behaviours in the presence of certain EBF doses, the infection with H. defensa did not significantly modify the escape behaviour and only marginally influenced the locomotor behaviour at high doses of EBF. Dose-response curves of EAG amplitudes after stimulation with EBF differed significantly between aphid genotypes in correlation with behavioural differences, whereas antennal sensitivity to EBF did not change significantly as a function of the symbiotic status. The protective symbiont H. defensa does thus not modify the olfactory sensitivity to the alarm pheromone. How EBF sensitivity is modified between genotypes or biotypes remains to be investigated.

Microbial associates are widespread in insects, some conferring a protection to their hosts against natural enemies like parasitoids. These protective symbionts may affect the infection success of the parasitoid by modifying behavioral defenses of their hosts, the development success of the parasitoid by conferring a resistance against it or by altering life-history traits of the emerging parasitoids. Here, we assessed the effects of different protective bacterial symbionts on the entire sequence of the host-parasitoid interaction (i.e. from parasitoid attack to offspring emergence) between the pea aphid, Acyrthosiphon pisum, and its main parasitoid, Aphidius ervi and their impacts on the life-history traits of the emerging parasitoids. To test whether symbiont-mediated phenotypes were general or specific to particular aphid-symbiont associations, we considered several aphid lineages, each harboring a different strain of either Hamiltonella defensa or Regiella insecticola, two protective symbionts commonly found in aphids. We found that symbiont species and strains had a weak effect on the ability of aphids to defend themselves against the parasitic wasps during the attack and a strong effect on aphid resistance against parasitoid development. While parasitism resistance was mainly determined by symbionts, their effects on host defensive behaviors varied largely from one aphid-symbiont association to another. Also, the symbiotic status of the aphid individuals had no impact on the attack rate of the parasitic wasps, the parasitoid emergence rate from parasitized aphids nor the life-history traits of the emerging parasitoids. Overall, no correlations between symbiont effects on the different stages of the host-parasitoid interaction was observed, suggesting no trade-offs or positive associations between symbiont-mediated phenotypes. Our study highlights the need to consider various sequences of the host-parasitoid interaction to better assess the outcomes of protective symbioses and understand the ecological and evolutionary dynamics of insect-symbiont associations.

post-print; International audience; Microbial endosymbiontsalter the phenotype of their host which may have cascading effects at both population and community levels. However, we currently lack information on whether the effects of viruses on both host phenotypic traits and host population demography can modify interactions with upper trophic levels. To fill this gap, we investigated whether a prevalent densovirus infecting the aphid Myzus persicae(i.e. MpDNV) can modify trophic interactions between host aphids and their natural enemies (i.e. predators and parasitoids) by influencing aphid phenotypic traits (i.e. body mass and defensive behaviours), population demography (i.e. density and age-structure) and susceptibility towards both predation and parasitism. We found that the virus decreased aphid body mass but did not influence their behavioural defences. At the population level,the virus had a minor effect on aphid adult mortality whereas it strongly reduced the density of nymphs and influenced the stage structure of aphid populations. In addition, the virusenhanced the susceptibility of aphids to parasitism regardless of the parasitoid species. Predation rate on adult aphids was not influenced by the virus but ladybeetle predators strongly decreased the number of aphid nymphs, especially for uninfected ones compared to infected ones. As a result, the virus decreased predator effect on aphid populations. By reducing both aphid quality and availability, increasing their susceptibility to parasitism, and modulating predator effect on aphid populations, we highlighted that viral endosymbionts can be prevalent drivers of their host ecology as they modify their phenotypes and interspecific interactions. These virus-mediated ecological effects may have consequences on enemies foraging strategies as well as trophic webs dynamics and structure.

Arctic ecosystems are subjected to strong environmental constraints that prevent both the colonization and development of many organisms. In Svalbard, few aphid species have established permanent populations. These high arctic aphid species have developed peculiar life-history traits such as shortened life cycles and reduced dispersal capacities. Here, we present data on the distribution and population genetics of Acyrthosiphon svalbardicum in Spitsbergen, the main island of the Svalbard archipelago, and compared its genetic structure with that of its close relative Acyrthosiphon brevicorne, sampled in the top of Scandinavian mainland. We found that A. svalbardicum is common but heterogeneously distributed along the west coast of Spitsbergen. We recorded this species up to 79&deg, 12&rsquo, which constitutes the northernmost location for any aphid. Genetic structure examined using microsatellite markers showed more pronounced spatial differentiation in A. svalbardicum than in A. brevicorne populations, presumably due to reduced dispersal capacities in the former species. Although populations of A. brevicorne and A. svalbardicum were well-delineated at nuclear loci, they shared similar cytoplasmic DNA haplotypes as revealed by sequence analysis of two DNA barcodes. These results raise questions about whether these two taxa are different species, and the colonization sources and history of the Svalbard archipelago by A. svalbardicum.

International audience; Microbial endosymbionts alter the phenotype of their host which may have cascading effects at both population and community levels. However, we currently lack information on whether the effects of viruses on both host phenotypic traits and host population demography can modify interactions with upper trophic levels. To fill this gap, we investigated whether a prevalent densovirus infecting the aphid Myzus persicae (i.e. MpDNV) can modify trophic interactions between host aphids and their natural enemies (i.e. predators and parasitoids) by influencing aphid phenotypic traits (i.e. body mass and defensive behaviours), population demography (i.e. density and age-structure) and susceptibility towards both predation and parasitism. We found that the virus decreased aphid body mass but did not influence their behavioural defences. At the population level, the virus had a minor effect on aphid adult mortality whereas it strongly reduced the density of nymphs and influenced the stage structure of aphid populations. In addition, the virus enhanced the susceptibility of aphids to parasitism regardless of the parasitoid species. Predation rate on adult aphids was not influenced by the virus but ladybeetle predators strongly decreased the number of aphid nymphs, especially for uninfected ones compared to infected ones. As a result, the virus decreased predator effect on aphid populations. By reducing both aphid quality and availability, increasing their susceptibility to parasitism, and modulating predator effect on aphid populations, we highlighted that viral endosymbionts can be prevalent drivers of their host ecology as they modify their phenotypes and interspecific interactions. These virus-mediated ecological effects may have consequences on enemies foraging strategies as well as trophic webs dynamics and structure.

International audience