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In this study the host plant genotype effect on cabbage aphid, Brevicoryne brassicae (L.)(Hemiptera: Aphididae) preference and performance, the effect of aphid genotype on parasitoids performance, as well as the indirect effects of plant genotypes on aphid parasitoid performance, were tested using different population samples of the aphid and its primary endoparasitoid wasp, Diaeretiella rapae (M'Intosh) (Hymenoptera: Braconidae). Experiments were run as fully-factorial randomized block design in a greenhouse. Accordingly, host plant cultivar had significant effects on the total number of aphids and aphid-load whilst the fitness of the aphid genotypes were also influenced by plant cultivar. The effect of parasitism on cabbage aphids was significantly different between plant cultivars. Overall, the results revealed that cabbage aphid is under different selective pressures arising from both higher (parasitoid) and lower (host plant cultivar) trophic levels. The host plant cultivar had a significant effect on both aphid fitness and parasitism rate on particular aphid genotypes. This indicates that host-plant-adapted aphid species can create much context-dependency in the nature and strength of ‘fitness benefits parasitism’, which may in turn alter the costs and benefits of host specialization.

Heritable symbionts are common in insects with many contributing to host defence. Hamiltonella defensa is a facultative, bacterial symbiont of the pea aphid, Acyrthosiphon pisum that provides protection against the endoparasitoid wasp Aphidius ervi. Protection levels vary among strains of H. defensa that are differentially infected by bacteriophages named APSEs. By contrast, little is known about mechanism(s) of resistance owing to the intractability of host-restricted microbes for functional study. Here, we developed methods for culturing strains of H. defensa that varied in the presence and type of APSE. Most H. defensa strains proliferated at 27°C in co-cultures with the TN5 cell line or as pure cultures with no insect cells. The strain infected by APSE3, which provides high levels of protection in vivo, produced a soluble factor(s) that disabled development of A. ervi embryos independent of any aphid factors. Experimental transfer of APSE3 also conferred the ability to disable A. ervi development to a phage-free strain of H. defensa. Altogether, these results provide a critical foundation for characterizing symbiont-derived factor(s) involved in host protection and other functions. Our results also demonstrate that phage-mediated transfer of traits provides a mechanism for innovation in host restricted symbionts.

Plants respond to insect attack by releasing blends of volatile chemicals that attract their herbivores’ specific natural enemies, while insect herbivores may carry endosymbiotic microorganisms that directly improve herbivore survival after natural enemy attack. Here we demonstrate that the two phenomena can be linked. Plants fed upon by pea aphids release volatiles that attract parasitic wasps, and the pea aphid can carry facultative endosymbiotic bacteria that prevent the development of the parasitic wasp larva and thus markedly improve aphid survival after wasp attack. We show that these endosymbionts also attenuate the systemic release of volatiles by plants after aphid attack, reducing parasitic wasp recruitment and increasing aphid fitness. Our results reveal a novel mechanism through which symbionts can benefit their hosts and emphasise the importance of considering the microbiome in understanding insect ecological interactions. Bacterial symbionts are increasingly known to influence behaviour and fitness in insects. Here, Frago et al. show that plants fed on by aphids with symbionts have altered volatile chemical profiles, leading to reduced parasitoid attack of aphids.

Intraguild predation (IGP) is a crucial ecological interaction that influences the dynamics of natural enemies and affects the effectiveness of biological control. Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), an invasive predator, significantly impacts native predators through IGP in certain countries. Pyemotes zhonghuajia (Yu, Zhang & He) (Prostigmata: Pyemotidae), a small ectoparasitoid, parasitizes various pests from the orders Lepidoptera, Coleoptera, and Hemiptera. Although both natural enemies are essential in controlling pests like Neotoxoptera formosana (Takahashi) (Hemiptera: Aphididae), their interactions and effects on pest management remain poorly understood.The study investigates the functional response of H. axyridis to N. formosana, the lethal ability of P. zhonghuajia against N. formosana, and how intraguild interactions affect the mortality rates of both N. formosana and H. axyridis when exposed to P. zhonghuajia. Our findings revealed that H. axyridis exhibited a Holling type II functional response to N. formosana, with female adults being the most effective predators. Pyemotes zhonghuajia demonstrated significant lethality against N. formosana, particularly at higher mite densities. However, the presence of P. zhonghuajia also increased the mortality rate of H. axyridis, highlighting a parasitism-driven intraguild interaction in which the mite dominates the predator. These results challenge conventional views of predator–parasitoid dynamics and highlight the complexity of interactions among natural enemies in pest control systems.

Bacteriophages are known to carry key virulence factors for pathogenic bacteria, but their roles in symbiotic bacteria are less well understood. The heritable symbiont Hamiltonella defensa protects the aphid Acyrthosiphon pisum from attack by the parasitoid Aphidius ervi by killing developing wasp larvae. In a controlled genetic background, we show that a toxin-encoding bacteriophage is required to produce the protective phenotype. Phage loss occurs repeatedly in laboratory-held H. defensa-infected aphid clonal lines, resulting in increased susceptibility to parasitism in each instance. Our results show that these mobile genetic elements can endow a bacterial symbiont with benefits that extend to the animal host. Thus, phages vector ecologically important traits, such as defense against parasitoids, within and among symbiont and animal host lineages.

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.

The potato aphid Macrosiphum euphorbiae is one of many polyphagous crop pests involved in the transmission of insect-vectored pathogens. While their North American counterparts reproduce via cyclical parthenogenesis, UK populations of M. euphorbiae appear to persist asexually, resulting in the maintenance of several genotypes, with some demonstrating genotype-specific traits; this includes innate resistance to parasitism from the hymenopterous parasitoid wasp Aphidius ervi . The genetic and molecular basis for genotype-specific traits is often unknown. Here we present a chromosome scale assembly for a parasitoid-resistant clonal line of M. euphorbiae and provide insights into the genotypic composition and distribution of UK potato aphid populations using microsatellite and whole-genome sequencing (WGS) techniques, focusing on geographically separated potato crops within two distinct areas of the UK (Merseyside and Tayside). We show that the genome consists of five chromosomal blocks, has a total size of 560 Mbp and a highly complete BUSCO score (C: 98.0%). The sampled potato aphid populations were dominated by two genotypes, one of which is absent from commercial farm settings. While the genetic and molecular basis for genotype-specific traits is unknown, the M. euphorbiae genotype distribution suggests either an intolerance to farming practices, such as insecticide use, or a broader host range in some populations. WGS data highlighted the asexual clonal lifestyle of M. euphorbiae genotypes in the UK, resolving individuals to a higher resolution than using microsatellite data. WGS data also indicates that M. euphorbiae UK populations are the result of a previous hybridization event. The work presented here will provide useful information for integrated pest management of potato aphids, elaborating on the relationship between genotype diversity and functional traits such as parasitism and insecticide resistance, and host plant use, as well as providing more resources for further comparative genomics studies within the Aphididae.

The development of insecticide-resistance mechanisms in aphids has been associated with inhibitory, pleiotropic fitness costs. Such fitness costs have not yet been examined in the UK’s most damaging cereal aphid, Sitobion avenae (grain aphid) (Hemiptera: Aphididae). This study aimed to evaluate the fitness trade-offs of the insecticide-resistant S . avenae clone versus an insecticide-susceptible S . avenae clone. Additionally, the parasitoid, Aphidius ervi (Hymenoptera: Braconidae), was introduced to examine its potential as a biological control agent. This study found that insecticide-resistant clones had significantly lower population growth and individual relative growth rate. Furthermore, insecticide-resistant clones suffered from a significantly greater rate of parasitisation (mummification) compared to their insecticide-susceptible counterparts. The successfulness of the parasitoid as a biological control agent could prevent the spread of the insecticide-resistant genotype. However, for this to be possible, insecticide spraying regimes need to be moderated, and habitat modification and parasitoid manipulation must be considered.

1. Eukaryotes commonly host communities of heritable symbiotic bacteria, many of which are not essential for their hosts' survival and reproduction. There is laboratory evidence that these facultative symbionts can provide useful adaptations, such as increased resistance to natural enemies. However, we do not know how symbionts affect host fitness when the latter are subject to attack by a natural suite of parasites and pathogens. 2. Here, we test whether two protective symbionts, Regiella insecticola and Hamiltonella defensa, increase the fitness of their host, the pea aphid (Acyrthosiphon pisum), under natural conditions. 3. We placed experimental populations of two pea aphid lines, each with and without symbionts, in five wet meadow sites to expose them to a natural assembly of enemy species. The aphids were then retrieved and mortality from parasitoids, fungal pathogens and other causes assessed. 4. We found that both Regiella and Hamiltonella reduce the proportion of aphids killed by the specific natural enemies against which they have been shown to protect in laboratory and cage experiments. However, this advantage was nullified (Hamiltonella) or reversed (Regiella) by an increase in mortality from other natural enemies and by the cost of carrying the symbiont. Symbionts therefore affect community structure by altering the relative success of different natural enemies. 5. Our results show that protective symbionts are not necessarily advantageous to their hosts, and may even behave more like parasites than mutualists. Nevertheless, bacterial symbionts may play an important role in determining food web structure and dynamics.

1. The pea aphid, Acyrthosiphon pisum, maintains extreme variation in resistance to its most common parasitoid wasp enemy, Aphidius ervi, which is sourced from two known mechanisms: protective bacterial symbionts, most commonly Hamiltonella defensa, or endogenously encoded defences. We have recently found that individual aphids may employ each defence individually, occasionally both defences together, or neither. 2. In field populations, Hamiltonella-infected aphids are found at low to moderate frequencies and while less is known about the frequency of resistant genotypes, they show up less often than susceptible genotypes in field collections. To better understand these patterns, we sought to compare the strengths and costs of both types of defence, individually and together, in order to elucidate the selective pressures that maintain multi-modal defence mechanisms or that may favour one over the other. 3. We experimentally infected five aphid genotypes (two lowly and three highly resistant), each with two symbiont strains, Hamiltonella-APSE8 (moderate protection) and Hamiltonella-APSE3 (high protection). This resulted in three sublines per genotype: uninfected, +APSE8 and +APSE3. Each of the 15 total sublines was first subjected to a parasitism assay to determine its resistance phenotype and in a second experiment, a subset was chosen to compare fitness (fecundity and survivorship) in the presence and absence of parasitism 4. In susceptible aphid genotypes, parasitized sublines infected with Hamiltonella generally showed increased protection with direct fitness benefits, but clear infection costs to fitness in the absence of parasitism. In resistant genotypes, Hamiltonella infection rarely conferred additional protection, often further reduced fecundity and survivorship when enemy challenged, and resulted in constitutive fitness costs in the absence of parasitism. We also identified strong aphid genotype×symbiontstrain interactions, such that the best defensive strategy against parasitoids varied for each aphid genotype; one performed best with no protective symbionts, the others with particular strains of Hamiltonella. 5. This surprising variability in outcomes helps explain why Hamiltonella infection frequencies are often intermediate and do not strongly track parasitism frequencies in field populations. We also find that variation in endogenous traits, such as resist-ance, among host genotypes may offer redundancy and generally limit the invasion potential of mutualistic microbes in insects.