EXPERIMENTAL EVOLUTION OF PARASITOID INFECTIVITY ON SYMBIONT‐PROTECTED HOSTS LEADS TO THE EMERGENCE OF GENOTYPE SPECIFICITY

Host‐parasitoid interactions may lead to strong reciprocal selection for traits involved in host defense and parasitoid counterdefense. In aphids, individuals harboring the facultative bacterial endosymbiont, Hamiltonella defensa, exhibit enhanced resistance to parasitoid wasps. We used an experimental evolution approach to investigate the ability of the parasitoid wasp, Lysiphlebus fabarum, to adapt to the presence of H. defensa in its aphid host Aphis fabae. Sexual populations of the parasitoid were exposed for 11 generations to a single clone of A. fabae, either free of H. defensa or harboring artificial infections with three different isolates of H. defensa. Parasitoids adapted rapidly to the presence of H. defensa in their hosts, but this adaptation was in part specific to the symbiont isolate they were evolving against and did not result in an improved infectivity on all symbiont‐protected hosts. Comparisons of life‐history traits among the evolved lines of parasitoids did not reveal any evidence for costs of adaptation to H. defensa in terms of correlated responses that could constrain such adaptation. These results show that parasitoids readily evolve counter‐adaptations to heritable defensive symbionts of their hosts, but that different symbiont strains impose different evolutionary challenges. The symbionts thus mediate the host‐parasite interaction by inducing line‐by‐line genetic specificity.     

Effects of pea aphid secondary endosymbionts on aphid resistance and development of the aphid parasitoid Aphidius ervi: a correlative study

In order to reduce parasite‐induced mortality, hosts may be involved in mutualistic interactions in which the partner contributes to resistance against the parasite. The pea aphid, Acyrthosiphon pisum Harris (Hemiptera: Aphididae), harbours secondary bacterial endosymbionts, some of which have been reported to confer resistance against aphid parasitoids. Although this resistance often results in death of the developing parasitoid larvae, some parasitoid individuals succeed in developing into adults. Whether these individuals suffer from fitness reduction compared to parasitoids developing in pea aphid clones without symbionts has not been tested so far. Using 30 pea aphid clones that differed in their endosymbiont complement, we studied the effects of these endosymbionts on aphid resistance against the parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae: Aphidiinae), host–parasitoid physiological interactions, and fitness of emerging adult parasitoids. The number of symbiont species in an aphid clone was positively correlated with a number of resistance measurements but there were also clear symbiont‐specific effects on the host–parasitoid interaction. As in previous studies, pea aphid clones infected with Hamiltonella defensa Moran et al. showed resistance against the parasitoid. In addition, pea aphid clones infected with Regiella insecticola Moran et al. and co‐infections of H. defensa–Spiroplasma, R. insecticola–Spiroplasma, and R. insecticola–H. defensa showed reduced levels of parasitism and mummification. Parasitoids emerging from symbiont‐infected aphid clones often had a longer developmental time and reduced mass. The number of teratocytes was generally lower when parasitoids oviposited in aphid clones with a symbiont complement. Interestingly, unparasitized aphids infected with Serratia symbiotica Moran et al. and R. insecticola had a higher fecundity than unparasitized aphids of uninfected pea aphid clones. We conclude that in addition to conferring resistance, pea aphid symbionts also negatively affect parasitoids that successfully hatch from aphid mummies. Because of the link between aphid resistance and the number of teratocytes, the mechanism underlying resistance by symbiont infection may involve interference with teratocyte development.     

Impact of environmental stress on aphid clonal resistance to parasitoids: Role of Hamiltonella defensa bacterial symbiosis in association with a new facultative symbiont of the pea aphid

Resistance to endoparasitoids in aphids involves complex interactions between insect and microbial players. It is now generally accepted that the facultative bacterial symbiont Hamiltonella defensa of the pea aphid Acyrthosiphon pisum is implicated in its resistance to the parasitoid Aphidius ervi. It has also been shown that heat negatively affects pea aphid resistance, suggesting the thermosensitivity of its defensive symbiosis. Here we examined the effects of heat and UV-B on the resistance of A. pisum to A. ervi and we relate its stability under heat stress to different facultative bacterial symbionts hosted by the aphid. For six A. pisum clones harboring four different facultative symbiont associations, the impact of heat and UV-B was measured on their ability to resist A. ervi parasitism under controlled conditions. The results revealed that temperature strongly affected resistance, while UV-B did not. As previously shown, highly resistant A. pisum clones singly infected with H. defensa became more susceptible to parasitism after exposure to heat. Interestingly, clones that were superinfected with H. defensa in association with a newly discovered facultative symbiont, referred to as PAXS (pea aphid X-type symbiont), not only remained highly resistant under heat stress, but also expressed previously unknown, very precocious resistance to A. ervi compared to clones with H. defensa alone. The prevalence of dual symbiosis involving PAXS and H. defensa in local aphid populations suggests its importance in protecting aphid immunity to parasitoids under abiotic stress.     

Strong specificity in the interaction between parasitoids and symbiont‐protected hosts

Coevolution between hosts and parasites may promote the maintenance of genetic variation in both antagonists by negative frequency‐dependence if the host–parasite interaction is genotype‐specific. Here we tested for specificity in the interaction between parasitoids (Lysiphlebus fabarum) and aphid hosts (Aphis fabae) that are protected by a heritable defensive endosymbiont, the γ‐proteobacterium Hamiltonella defensa. Previous studies reported a lack of genotype specificity between unprotected aphids and parasitoids, but suggested that symbiont‐conferred resistance might exhibit a higher degree of specificity. Indeed, in addition to ample variation in host resistance as well as parasitoid infectivity, we found a strong aphid clone‐by‐parasitoid line interaction on the rates of successful parasitism. This genotype specificity appears to be mediated by H. defensa, highlighting the important role that endosymbionts can play in host–parasite coevolution.     

Diversity in symbiont consortia in the pea aphid complex is associated with large phenotypic variation in the insect host

Virtually all eukaryotes host microbial symbionts that influence their phenotype in many ways. In a host population, individuals may differ in their symbiotic complement in terms of symbiont species and strains. Hence, the combined expression of symbiont and host genotypes may generate a range of phenotypic diversity on which selection can operate and influence host population ecology and evolution. Here, we used the pea aphid to examine how the infection with various symbiotic complements contributes to phenotypic diversity of this insect species. The pea aphid hosts an obligate symbiont (Buchnera aphidicola) and several secondary symbionts among which is Hamiltonella defensa. This secondary symbiont confers a protection against parasitoids but can also reduce the host’s longevity and fecundity. These phenotypic effects of H. defensa infection have been described for a small fraction of the pea aphid complex which encompasses multiple plant-specialized biotypes. In this study, we examined phenotypic differences in four pea aphid biotypes where H. defensa occurs at high frequency and sometimes associated with other secondary symbionts. For each biotype, we measured the fecundity, lifespan and level of parasitoid protection in several aphid lineages differing in their symbiotic complement. Our results showed little variation in longevity and fecundity among lineages but strong differences in their protection level. These differences in protective levels largely resulted from the strain type of H. defensa and the symbiotic consortium in the host. This study highlights the important role of symbiotic complement in the emergence of phenotypic divergence among host populations of the same species.     

Evidence for specificity in symbiont-conferred protection against parasitoids

Many insects harbour facultative symbiotic bacteria, some of which have been shown to provide resistance against natural enemies. One of the best-known protective symbionts is Hamiltonella defensa, which in pea aphid (Acyrthosiphon pisum) confers resistance against attack by parasitoid wasps in the genus Aphidius (Braconidae). We asked (i) whether this symbiont also confers protection against a phylogenetically distant group of parasitoids (Aphelinidae) and (ii) whether there are consistent differences in the effects of bacteria found in pea aphid biotypes adapted to different host plants. We found that some H. defensa strains do provide protection against an aphelinid parasitoid Aphelinus abdominalis. Hamiltonella defensa from the Lotus biotype provided high resistance to A. abdominalis and moderate to low resistance to Aphidius ervi, while the reverse was seen from Medicago biotype isolates. Aphids from Ononis showed no evidence of symbiont-mediated protection against either wasp species and were relatively vulnerable to both. Our results may reflect the different selection pressures exerted by the parasitoid community on aphids feeding on different host plants, and could help explain the maintenance of genetic diversity in bacterial symbionts.     

Comparing constitutive and induced costs of symbiont‐conferred resistance to parasitoids in aphids

Host defenses against parasites do not come for free. The evolution of increased resistance can be constrained by constitutive costs associated with possessing defense mechanisms, and by induced costs of deploying them. These two types of costs are typically considered with respect to resistance as a genetically determined trait, but they may also apply to resistance provided by ‘helpers’ such as bacterial endosymbionts. We investigated the costs of symbiont‐conferred resistance in the black bean aphid, Aphis fabae (Scopoli), which receives strong protection against the parasitoid Lysiphlebus fabarum from the defensive endosymbiont Hamiltonella defensa. Aphids infected with H. defensa were almost ten times more resistant to L. fabarum than genetically identical aphids without this symbiont, but in the absence of parasitoids, they had strongly reduced lifespans, resulting in lower lifetime reproduction. This is evidence for a substantial constitutive cost of harboring H. defensa. We did not observe any induced cost of symbiont‐conferred resistance. On the contrary, symbiont‐protected aphids that resisted a parasitoid attack enjoyed increased longevity and lifetime reproduction compared with unattacked controls, whereas unprotected aphids suffered a reduction of longevity and reproduction after resisting an attack. This surprising result suggests that by focusing exclusively on the protection, we might underestimate the selective advantage of infection with H. defensa in the presence of parasitoids.     

Genotype‐by‐genotype specificity remains robust to average temperature variation in an aphid/endosymbiont/parasitoid system

Genotype‐by‐genotype interactions demonstrate the existence of variation upon which selection acts in host–parasite systems at respective resistance and infection loci. These interactions can potentially be modified by environmental factors, which would entail that different genotypes are selected under different environmental conditions. In the current study, we checked for a G × G × E interaction in the context of average temperature and the genotypes of asexual lines of the endoparasitoid wasp Lysiphlebus fabarum and isolates of Hamiltonella defensa, a protective secondary endosymbiont of the wasp's host, the black bean aphid Aphis fabae. We exposed genetically identical aphids harbouring different isolates of H. defensa to three asexual lines of the parasitoid and measured parasitism success under three different temperatures (15, 22 and 29 °C). Although there was clear evidence for increased susceptibility to parasitoids at the highest average temperature and a strong G × G interaction between the host's symbionts and the parasitoids, no modifying effect of temperature, that is, no significant G × G × E interaction, was detected. This robustness of the observed specificity suggests that the relative fitness of different parasitoid genotypes on hosts protected by particular symbionts remains uncomplicated by spatial or temporal variation in temperature, which should facilitate biological control strategies.     

Co‐occurrence of defensive traits in the potato aphid Macrosiphum euphorbiae

1. Insecticide usage selects strongly for resistance in aphid populations, but this could entail fitness costs in other resistance traits. The potato aphid Macrosiphum euphorbiae Thomas exhibits intraspecific variation in susceptibility to parasitism by braconid wasps and provides a suitable species to study the relation between the defensive traits of parasitism and insecticide resistance. 2. Clonal lines (23 in total) of M. euphorbiae were established from aphids collected in 2013 from geographically separate populations in the U.K. Clonal lines belonged to five aphid genotypes, but one genotype predominated (78% of samples), and the facultative endosymbiont Hamiltonella defensa was detected in c. 40% of lines. 3. Total esterase activity in aphid tissues varied significantly between aphid genotypes and collection areas, but there was no clear pattern in relation to H. defensa infection or between collection sites likely to differ in insecticide pressures. 4. Five clonal lines representing low to moderate levels of enzyme activity, which included different aphid genotypes and presence/absence of H. defensa infection, were assayed for their susceptibility to the parasitoid wasp Aphidius ervi Haliday. Aphid mummification varied significantly between aphid genotypes, with low values in one genotype of aphids irrespective of H. defensa presence. 5. The results revealed that aphid lines belonging to the parasitism‐resistant genotype exhibited moderate levels of total esterase activity, indicating a competitve advantage for this genotype of M. euphorbiae when exposed to chemical and biological control factors in agroecosystems.     

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.     

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 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.     

Estimating costs of aphid resistance to parasitoids conferred by a protective strain of the bacterial endosymbiont Regiella insecticola

Heritable bacterial endosymbionts are common in aphids (Hemiptera: Aphididae), and they can influence ecologically important traits of their hosts. It is generally assumed that their persistence in a population is dependent on a balance between the costs and benefits they confer. A good example is Hamiltonella defensa Moran et al., a facultative symbiont that provides a benefit by strongly increasing aphid resistance to parasitoid wasps, but becomes costly to the host in the absence of parasitoids. Regiella insecticola Moran et al. is another common symbiont of aphids and generally does not influence resistance to parasitoids. In the green peach aphid, Myzus persicae (Sulzer), however, one strain (R5.15) was discovered that behaves like H. defensa in that it provides strong protection against parasitoid wasps. Here we compare R5.15‐infected and uninfected lines of three M. persicae clones to test whether this protective symbiont is costly as well, i.e., whether it has any negative effects on aphid life‐history traits. Furthermore, we transferred R5.15 to two other aphid species, the pea aphid, Acyrthosiphon pisum (Harris), and the black bean aphid, Aphis fabae Scopoli, where this strain is also protective against parasitoids and where we could compare its effects with those of additional, non‐protective strains of R. insecticola. Negative effects of R5.15 on host survival and lifetime reproduction were limited and frequently non‐significant, and these effects were comparable or in one case weaker than those of R. insecticola strains that are not protective against parasitoid wasps. Unless the benefit of protection is counteracted by detrimental effects on traits that were not considered in this study, R. insecticola strain R5.15 should have a high potential to spread in aphid populations.     

Cheaper is not always worse: strongly protective isolates of a defensive symbiont are less costly to the aphid host

Defences against parasites are typically associated with costs to the host that contribute to the maintenance of variation in resistance. This also applies to the defence provided by the facultative bacterial endosymbiont Hamiltonella defensa, which protects its aphid hosts against parasitoid wasps while imposing life-history costs. To investigate the cost–benefit relationship within protected hosts, we introduced multiple isolates of H. defensa to the same genetic backgrounds of black bean aphids, Aphis fabae, and we quantified the protection against their parasitoid Lysiphlebus fabarum as well as the costs to the host (reduced lifespan and reproduction) in the absence of parasitoids. Surprisingly, we observed the opposite of a trade-off. Strongly protective isolates of H. defensa reduced lifespan and lifetime reproduction of unparasitized aphids to a lesser extent than weakly protective isolates. This finding has important implications for the evolution of defensive symbiosis and highlights the need for a better understanding of how strain variation in protective symbionts is maintained.     

Parasitoids as drivers of symbiont diversity in an insect host

Immune systems have repeatedly diversified in response to parasite diversity. Many animals have outsourced part of their immune defence to defensive symbionts, which should be affected by similar evolutionary pressures as the host’s own immune system. Protective symbionts provide efficient and specific protection and respond to changing selection pressure by parasites. Here we use the aphid Aphis fabae, its protective symbiont Hamiltonella defensa, and its parasitoid Lysiphlebus fabarum to test whether parasite diversity can maintain diversity in protective symbionts. We exposed aphid populations with the same initial symbiont composition to parasitoid populations that differed in their diversity. As expected, single parasitoid genotypes mostly favoured a single symbiont that was most protective against that particular parasitoid, while multiple symbionts persisted in aphids exposed to more diverse parasitoid populations, which in turn affected aphid population density and rates of parasitism. Parasite diversity may be crucial to maintaining symbiont diversity in nature.     

Mobile elements create strain-level variation in the services conferred by an aphid symbiont

Heritable, facultative symbionts are common in arthropods, often functioning in host defence. Despite moderately reduced genomes, facultative symbionts retain evolutionary potential through mobile genetic elements (MGEs). MGEs form the primary basis of strain-level variation in genome content and architecture, and often correlate with variability in symbiont-mediated phenotypes. In pea aphids (Acyrthosiphon pisum), strain-level variation in the type of toxin-encoding bacteriophages (APSEs) carried by the bacterium Hamiltonella defensa correlates with strength of defence against parasitoids. However, co-inheritance creates difficulties for partitioning their relative contributions to aphid defence. Here we identified isolates of H. defensa that were nearly identical except for APSE type. When holding H. defensa genotype constant, protection levels corresponded to APSE virulence module type. Results further indicated that APSEs move repeatedly within some H. defensa clades providing a mechanism for rapid evolution in anti-parasitoid defences. Strain variation in H. defensa also correlates with the presence of a second symbiont Fukatsuia symbiotica. Predictions that nutritional interactions structured this coinfection were not supported by comparative genomics, but bacteriocin-containing plasmids unique to co-infecting strains may contribute to their common pairing. In conclusion, strain diversity, and joint capacities for horizontal transfer of MGEs and symbionts, are emergent players in the rapid evolution of arthropods.     

Cascading effects of herbivore protective symbionts on hyperparasitoids

1. Microbial symbionts can play an important role in defending their insect hosts against natural enemies. However, researchers have little idea how the presence of such protective symbionts impacts food web interactions and species diversity. 2. This study investigated the effects of a protective symbiont (Hamiltonella defensa) in pea aphids (Acyrthosiphon pisum) on hyperparasitoids, which are a trophic level above the natural enemy target of the symbiont (primary parasitoids). 3. Pea aphids, with and without their natural infections of H. defensa, were exposed first to a primary parasitoid against which the symbiont provides partial protection (either Aphidius ervi or Aphelinus abdominalis), and second to a hyperparasitoid known to attack the primary parasitoid species. 4. It was found that hyperparasitoid hatch rate was substantially affected by the presence of the symbiont. This effect appears to be entirely due to the removal of potential hosts by the action of the symbiont: there was no additional benefit or cost experienced by the hyperparasitoids in response to symbiont presence. The results were similar across the two different aphid–parasitoid–hyperparasitoid interactions we studied. 5. It is concluded that protective symbionts can have an important cascading effect on multiple trophic levels by altering the success of natural enemies, but that there is no evidence for more complex interactions. These findings demonstrate that the potential influence of protective symbionts on the wider community should be considered in future food web studies.     

Symbiont‐conferred protection against Hymenopteran parasitoids in aphids: how general is it?

1. Hosts are often targeted by multiple species of parasites, leading to a confluence of selective pressures on them. In response, hosts may either evolve defences that act very generally, or specific defences against particular parasites. Aphids are attacked by multiple species of endoparasitoid wasps, and there is clear evidence that heritable endosymbionts can confer resistance against some of these wasps. Less clear is how symbiont‐conferred resistance in a single host acts against multiple parasitoid species. 2. This question was addressed in the black bean aphid, Aphis fabae (Scopoli). Unprotected aphids and aphids protected by three different strains of the defensive endosymbiont Hamiltonella defensa were exposed to four species of parasitic wasps: the parthenogenetic species Lysiphlebus fabarum (Marshall), which was represented by three different asexual lines, and the sexual species Aphidius colemani (Viereck), Binodoxys angelicae (Halliday), and Aphelinus chaonia (Walker). 3. Hamiltonella defensa provided strong protection against L. fabarum and Aphidius colemani, but there was no evidence that H. defensa‐infected aphids were more resistant to the other parasitoid species. While Aphidius colemani was virtually unable to parasitise any aphids harbouring H. defensa, there was variation among the three asexual lines of L. fabarum in how susceptible they were to the defence provided by the different symbiont strains, resulting in a significant genotype‐by‐genotype interaction. 4. The present results suggest that symbiosis with H. defensa does not provide aphids with a general defence against parasitoid wasps, possibly because some species have evolved specific counter adaptations or because biological differences preclude the symbiont's effectiveness against these species.     

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 transmission 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 have achieved this by evolving the ability to protect their hosts against parasitoids. Reviewing empirical work and some models, I explore the evolutionary ecology of symbiont‐conferred resistance to parasitoids in order to understand how defensive symbiont frequencies are maintained at the intermediate levels observed in aphid populations. I further show that defensive symbionts alter the reciprocal selection between aphids and parasitoids by augmenting the heritable variation for resistance, by increasing the genetic specificity of the host–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 by exploiting the parasitoids’ demonstrated ability to rapidly evolve counteradaptations to symbiont‐conferred resistance.     

Horizontal transfer of facultative endosymbionts is limited by host relatedness

Heritable microbial symbionts can have important effects on many aspects of their hosts’ biology. Acquisition of a novel symbiont strain can provide fitness benefits to the host, with significant ecological and evolutionary consequences. We measured barriers to horizontal transmission by artificially transferring facultative symbionts from the grain aphid, Sitobion avenae, and five other aphid species into two clonal genotypes of S. avenae. We found the symbiont Hamiltonella defensa establishes infections more easily following a transfer from the same host species and that such infections are more stable. Infection success was also higher when the introduced symbiont strain was more closely related to the strain that was originally present in the host (but which had previously been removed). There were no differences among successfully established symbiont strains in their effect on aphid fecundity. Hamiltonella defensa did not confer protection against parasitoids in our S. avenae clones, although it often does in other aphid hosts. However, strains of the symbiont Regiella insecticola originating from two host species protected grain aphids against the pathogenic fungus Pandora neoaphidis. This study helps describe the extent to which facultative symbionts can act as a pool of adaptations that can be sampled by their eukaryote hosts.     

Does sex-biased dispersal account for the lack of geographic and host-associated differentiation in introduced populations of an aphid parasitoid?

Host recognition and use in female parasitoids strongly relies on host fidelity, a plastic behavior which can significantly restrict the host preferences of parasitoids, thus reducing the gene flow between parasitoid populations attacking different insect hosts. However, the effect of migrant males on the genetic differentiation of populations has been frequently ignored in parasitoids, despite its known impact on gene flow between populations. Hence, we studied the extent of gene flow mediated by female and male parasitoids by assessing sibship relationships among parasitoids within and between populations, and its impact on geographic and host‐associated differentiation in the aphid parasitoid Aphidius ervi. We report evidences of a high gene flow among parasitoid populations on different aphid hosts and geographic locations. The high gene flow among parasitoid populations was found to be largely male mediated, suggested by significant differences in the distribution of full‐sib and paternal half‐sib dyads of parasitoid populations.