Coinfection of the secondary symbionts,Hamiltonella defensa and Arsenophonus sp.contribute to the performance of the major aphid pest,Aphis gossypii(Hemiptera:Aphididae)

Bacterial endosymbionts play important roles in ecological traits of aphids.In this study,we characterize the bacterial endosymbionts of A.gossypii collected in Karaj,Iran and their role in the performance of the aphid.Our results indicated that beside Buchnera aphidicola,A.gossypii,also harbors both Hamiltonella defensa and Arsenophonus sp.Quantitative PCR(qPCR)results revealed that the populations of the endosymbionts increased throughout nymphal development up to adult emergence;thereafter,populations of Buchnera and Arsenophonus were diminished while the density of H.defensa constantly increased.Buchnera reduction caused prolonged development and no progeny production.Furthermore,secondary symbiont reduction led to reduction of the total life span and intrinsic rate of natural increase as well as appearance of the deformed dead offspring in comparison with the control insects.Reduction of the secondary symbionts did not affect parasitism rate of the aphid by the parasitic wasp Aphidius matricariae.Together these findings showed that H.defensa and Arsenophonus contributed to the fitness of A.gossypii by enhancing its performance,but not through parasitoid resistance.

The evolutionary ecology of symbiont-conferred resistance to parasitoids in aphids

Aphids may harbor a wide variety of facultative bacterial endosymbionts. These symbionts are transmitted maternally with high fidelity and they show horizontal trans-mission as well, albeit at rates too low to enable infectious spread. Such symbionts need to provide a net fitness benefit to their hosts to persist and spread. Several symbionts haveachieved this by evolving the ability to protect their hosts against parasitoids. Reviewing empirical work and some models, I explore the evolutionary ecology of symbiont-conferredresistance to parasitoids in order to understand how defensive symbiont frequencies are maintained at the intermediate levels observed in aphid populations. I further show thatdefensive symbionts alter the reciprocal selection between aphids and parasitoids by augmenting the heritable variation for resistance, by increasing the genetic specificity of thehost-parasitoid interaction, and by inducing environment-dependent trade-offs. These effects are conducive to very dynamic, symbiont-mediated coevolution that is driven by frequency-dependent selection. Finally I argue that defensive symbionts represent a problem for biological control of pest aphids, and I propose to mitigate this problem byexploiting the parasitoids＇ demonstrated ability to rapidly evolve counteradaptations to symbiont-conferred resistance.

The price of protection:a defensive endosymbiont impairs nymph growth in the bird cherry-oat aphid,Rhopalosiphum padi

Bacterial endosymbionts have enabled aphids to adapt to a range of stressors,but their effects in many aphid species remain to be established.The bird cherry-oat aphid,Rhopalosiphum padi(Linnaeus),is an important pest of cereals worldwide and has been reported to form symbiotic associations with Serratia symbiotica and Sitobion miscanthi L-type symbiont endobacteria,although the resulting aphid phenotype has not been described.This study presents the first report of R.padi infection with the facultative bacterial endosymbiont Hamiltonella defensa.Individuals of R.padi were sampled from populations in Eastern Scotland,UK,and shown to represent seven R.padi genotypes based on the size of polymorphic microsatellite markers;two of these genotypes harbored H.defensa.In parasitism assays,survival of H.defensa-infected nymphs following attack by the parasitoid wasp Aphidius colemani(Viereck)was 5 fold higher than for uninfected nymphs.Aphid genotype was a major determinant of aphid performance on two Hordeum species,a modern cultivar of barley H.vulgare and a wild relative H.spontaneum,although aphids infected with H.defensa showed 16%lower nymph mass gain on the partially resistant wild relative compared with uninfected individuals.These findings suggest that deploying resistance traits in barley will favor the fittest R.padi genotypes,but symbiontinfected individuals will be favored when parasitoids are abundant,although these aphids will not achieve optimal performance on a poor quality host plant.

Consequences of coinfection with protective symbionts on the host phenotype and symbiont titres in the pea aphid system

Symbiotic associations between microbes and insects are widespread, and it is frequent that several symbionts share the same host individual. Hence, interactions can occur between these symbionts, influencing their respective abundance within the host with consequences on its phenotype. Here, we investigate the effects of multiple infections in the pea aphid, Acyrthosiphon pisurn, which is the host of an obligatory and several facultative symbionts. In particular, we study the influence of a coinfection with 2 protective symbionts： Harniltonella defensa, which confers protection against parasitoids, and Rickettsiella viridis, which provides protection against fungal pathogens and predators. The effects of Hamiltonella-Rickettsiella coinfection on the respective abundance of the symbionts, host fitness and efficacy of enemy protection were studied. Asymmetrical interactions between the 2 protective symbionts have been found： when they coinfect the same aphid individuals, the Rickettsiella infection affected Hamiltonella abundance within hosts but not the Hamiltonella-mediated protective phenotype while the Hamiltonella infection negatively influences the Rickettsiella-mediated protective phenotype but not its abundance. Harboring the 2 protective symbionts also reduced the survival and fecundity of host individuals. Overall, this work highlights the effects of multiple infections on symbiont abundances and host traits that are likely to impact the maintenance of the symbiotic associations in natural habitats.

Influence of"protective"symbionts throughout the different steps of an aphid-parasitoid interaction

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 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.