Assessment of the risk of imidaclothiz to the dominant aphid parasitoid Binodoxys communis (Hymenoptera: Braconidae).

The neonicotinoid of imidaclothiz insecticide with low resistance and high efficiency, has great potential for application in pest control in specifically cotton field. In this systematically evaluate the effects of sublethal doses of imidaclothiz (LC10: 11.48 mg/L; LC30: 28.03 mg/L) on the biology, transcriptome, and microbiome of Binodoxys communis, the predominant primary parasitic natural enemy of aphids. The findings indicated that imidaclothiz has significant deleterious effects on the survival rate, parasitic rate, and survival time of B. communis. Additionally, there was a marked reduction in the survival rate and survival time of the F1 generation, that is, the negative effect of imidaclothiz on B. communis was continuous and trans-generational. Transcriptome analysis revealed that imidaclothiz treatment elicited alterations in the expression of genes associated with energy and detoxification metabolism. In addition, 16S rRNA analysis revealed a significant increase in the relative abundance of Rhodococcus and Pantoea, which are associated with detoxification metabolism, due to imidaclothiz exposure. These findings provide evidence that B. communis may regulate gene expression in conjunction with symbiotic bacteria to enhance adaptation to imidaclothiz. Finally, this study precise evaluation of imidaclothiz's potential risk to B. communis and provides crucial theoretical support for increasing the assessment of imidaclothiz in integrated pest management.

Transgenerational phenotypic plasticity of diapause induction and related fitness cost in a commercial strain of the parasitoid Aphidius ervi Haliday.

Diapause is an adaptation that insects have evolved to synchronize their life cycle with that of seasonal climatic changes and resources availability. However, cues for its induction are not always clear and, in some cases, a maternal effect may be involved. At the population level, just a part of the individuals may exhibit diapause with important consequences in terms of winter survival. Moreover, clear indicators of diapause state are difficult to identify. Diapause induction was thus investigated in the aphid parasitoid species Aphidius ervi Haliday (Hymenoptera: Braconidae) developing in the aphid Sitobion avenae (Hemiptera: Aphididae) at four crossed photothermal regimes (16 °C and 8 °C, 16:8 h L:D and 8:16 h L:D), and during 2 successive generations. We analyzed the reliability of changes in mummy color to assess for the diapausing state compared to dissections, and we measured parasitoid morphological and physiological traits. We observed that the proportion of dark brown mummies increased after one generation under low photothermal regime compared to other regimes. No diapause was recorded at 16 °C, 16:8 h L:D, while we observed 16.2% and 67.5% diapause incidence at 8 °C, 8:16 h L:D, at 1st and 2nd generation, respectively. Diapause induction is thus increased by short day-length conditions and low temperatures as well as by maternal effects. All parasitoid life-history traits (weight, size, fat content, water content, egg-load, and longevity) were affected by the photothermal regime and/or the generation. These results raise new questions on the environmental thresholds needed to induce diapause and on survival and adaptation potential of commercially available parasitoid strains in different environments.

Evolutionary costs and benefits of infection with diverse strains of Spiroplasma in pea aphids.

The heritable endosymbiont Spiroplasma infects many insects and has repeatedly evolved the ability to protect its hosts against different parasites. Defenses do not come for free to the host, and theory predicts that more costly symbionts need to provide stronger benefits to persist in host populations. We investigated the costs and benefits of Spiroplasma infections in pea aphids (Acyrthosiphon pisum), testing 12 bacterial strains from three different clades. Virtually all strains decreased aphid lifespan and reproduction, but only two had a (weak) protective effect against the parasitoid Aphidius ervi, an important natural enemy of pea aphids. Spiroplasma-induced fitness costs were variable, with strains from the most slowly evolving clade reaching higher titers and curtailing aphid lifespan more strongly than other strains. Some Spiroplasma strains shared their host with a second endosymbiont, Regiella insecticola. Although the result of an unfortunate handling error, these co-infections proved instructive, because they showed that the cost of infection with Spiroplasma may be attenuated in the presence of Regiella. These results suggest that mechanisms other than protection against A. ervi maintain pea aphid infections with diverse strains of Spiroplasma, and that studying them in isolation will not provide a complete picture of their effects on host fitness.

Multi-modal defences in aphids offer redundant protection and increased costs likely impeding a protective mutualism.

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. 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. 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. 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 × symbiont-strain 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. 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 resistance, among host genotypes may offer redundancy and generally limit the invasion potential of mutualistic microbes in insects.

Cornicle secretions by Aphis fabae (Hemiptera: Aphididae) result in age-dependent costs and improved host suitability for Lysiphlebus fabarum (Marshall) (Hymenoptera: Braconidae).

We examined the life history consequences of cornicle secretion by Aphis fabae Scopoli in second and fourth instars, and its effects on host suitability for its parasitoid, Lysiphlebus fabarum (Marshall). Cornicle secretion did not affect aphid fecundity, but secretion in the second instar enhanced life table parameters, whereas secretion in the fourth instar affected them negatively, suggesting a higher cost of secretion in later instars. Secretion in either instar improved host suitability for L. fabarum. Although control and treated aphids were parasitized at similar rates, and with similar success, wasps developed faster and emerged as larger adults in aphids that had secreted, regardless of instar. Transgenerational effects were also evident. Progeny emergence was higher when parental wasps developed in fourth instars than in seconds, whether aphids secreted or not, and progeny were larger when parental hosts secreted in the second instar, but not in the fourth. Secreting fourth instars were preferred to controls by L. fabarum females in choice tests, but not secreting second instars, and fourth-instar secretion improved wasp emergence. When control aphids were attacked, second instars were more likely to secrete than fourth instars, whereas the latter were more likely to kick the parasitoid. Cornicle secretion reduced the probability of subsequent secretion events and the frequency of other aphid defensive behaviors, indicating energetic tradeoffs among defensive tactics. Overall, our results revealed that cornicle secretion by immature A. fabae exacts both physiological and behavioral costs and results in improved host suitability for its parasitoid.

Trade-Off Between Fitness Gain and Cost Determines Profitability of a Peach Aphid Parasitoid.

Aphidius colemani (Viereck) (Hymenoptera: Aphidiidae) is commercially produced and utilized for biological control of peach aphid Myzus persicae (Sulzer) (Hemiptera: Aphididae) on greenhouse crops in many countries. To provide knowledge for the evaluation of parasitoid-host interactions and development of effective mass rearing programs, we investigated how and why host age or size affected fitness gain in A. colemani We show that the parasitoid was significantly more likely to encounter larger hosts and that an encounter almost always triggered an attack attempt. However, the attack attempt did not proportionally translate into oviposition because larger aphids had greater ability to defend themselves and the parasitoid spent more time in handling larger aphids. The host age at parasitization had no effect on emergence rates and sex ratio of parasitoid progeny, suggesting that pupae and larvae have similar survival rate in hosts of different ages and/or the parasitoid females do not adjust sex allocation based on host size. When parasitizing mid-aged hosts, the parasitoid gained maximum fitness for their progeny in developmental period, body size, and parasitism. Taking all findings together, we suggest that parasitizing mid-aged green peach aphid nymphs is most profitable for A. colemani.

Placenta-like structure of the aphid endoparasitic wasp Aphidius ervi: a strategy of optimal resources acquisition.

Aphidius ervi (Hymenoptera: Braconidae) is an entomophagous parasitoid known to be an effective parasitoid of several aphid species of economic importance. A reduction of its production cost during mass rearing for inundative release is needed to improve its use in biological control of pests. In these contexts, a careful analysis of its entire development phases within its host is needed. This paper shows that this parasitoid has some characteristics in its embryological development rather complex and different from most other reported insects, which can be phylogenetically very close. First, its yolkless egg allows a high fecundity of the female but force them to hatch from the egg shell rapidly to the host hemocoel. An early cellularisation allowing a rapid differentiation of a serosa membrane seems to confirm this hypothesis. The serosa wraps the developing embryo until the first instar larva stage and invades the host tissues by microvilli projections and form a placenta like structure able to divert host resources and allowing nutrition and respiration of embryo. Such interspecific invasion, at the cellular level, recalls mammal's trophoblasts that anchors maternal uterine wall and underlines the high adaptation of A. ervi to develop in the host body.

Genetic covariation between effectiveness and cost of defence in aphids.

Ecological immunology distinguishes between the long-term evolutionary costs of possessing defences against parasites and the short-term costs of using them. Evolutionary biologists have typically focused on the former in the search for constraints on the evolution of resistance. Here, we show in the peach-potato aphid, Myzus persicae, that short-term costs may be of equal evolutionary importance. Survivors of more resistant aphid clones suffered a higher reduction of fecundity upon parasitoid attack than survivors of more susceptible clones. This genetically based trade-off between benefits and costs of defence may limit the evolution of increased resistance and explain the maintenance of genetic variation for resistance under environmental variation in parasitism risk.

Efficacy assessment of Aphidius colemani (Hymenoptera: Braconidae) for suppression of Aphis gossypii (Homoptera: Aphididae) in greenhouse-grown chrysanthemum.

To assess biological control as a management tool for the cotton aphid, Aphis gossypii Glover (Homoptera: Aphididae), the efficacy of Aphidius colemani Viereck (Hymenoptera: Braconidae) for suppression of A. gossypii in greenhouse-grown chrysanthemums, Dendranthema grandiflora (Tzvelev), was compared with a pesticide standard, imidacloprid (Marathon 1% G) and an untreated check. No significant differences were found between aphid populations in the two treatments. A. colemani and imidacloprid kept aphid numbers very low, with the correspondent aphid populations exhibiting very low intrinsic rates of increase (r(m) = -0.0369 and r(m) = 0.0151, respectively), in contrast to the exponential growth of aphid populations (r(m) = 0.1085) observed on the untreated plants. Parasitism levels in A. colemani plots ranged from 48.93 to 83.38%. Esthetic damage parameters, including exuviae, honeydew, and sooty mold on leaves, were significantly different between treatments and untreated control, and damage levels were minimal with the insecticide treatment and natural enemy releases. The cost of A. colemani releases was 4.7 times greater than the cost of the imidacloprid treatment.

Costs and benefits of a superinfection of facultative symbionts in aphids.

Symbiotic associations between animals and inherited micro-organisms are widespread in nature. In many cases, hosts may be superinfected with multiple inherited symbionts. Acyrthosiphon pisum (the pea aphid) may harbour more than one facultative symbiont (called secondary symbionts) in addition to the obligate primary symbiont, Buchnera aphidicola. Previously we demonstrated that, in a controlled genetic background, A. pisum infected with either Serratia symbiotica or Hamiltonella defensa (called R- and T-type in that study) were more resistant to attack by the parasitoid Aphidius ervi. Here, we examined the consequences of A. pisum superinfected with both resistance-conferring symbionts. We found that an A. pisum line co-infected with both S. symbiotica and H. defensa symbionts exhibits even greater resistance to parasitism by A. ervi than either of the singly infected lines. Despite this added benefit to resistance, superinfections of S. symbiotica and H. defensa symbionts appeared rare in our survey of Utah A. pisum symbionts, which is probably attributable to severe fecundity costs. Quantitative polymerase chain reaction estimates indicate that while the density of H. defensa is similar in singly and superinfected hosts, S. symbiotica densities increased dramatically in superinfected hosts. Over-proliferation of symbionts or antagonistic interactions between symbionts may be harmful to the aphid host. Our results indicate that in addition to host-symbiont interactions, interactions among the symbionts themselves probably play a critical role in determining the distributions of symbionts in natural populations.

Resistance is costly: trade-offs between immunity, fecundity and survival in the pea aphid.

Parasitoids are among the most important natural enemies of insects in many environments. Acyrthosiphon pisum, the pea aphid, is a common pest of the leguminous crops in temperate regions. Pea aphids are frequently attacked by a range of endoparasitic wasps, including the common aphidiine, Aphidius ervi. Immunity to parasitoid attack is thought to involve secondary symbiotic bacteria, the presence of which is associated with the death of the parasitoid egg. It has been suggested that there is a fecundity cost of resistance, as individuals carrying the secondary symbionts associated with parasitoid resistance have fewer offspring. Supporting this hypothesis, we find a positive relationship between fecundity and susceptibility to parasitoid attack. There is also a negative relationship between fecundity and off-plant survival time (which positively correlates with resistance to parasitoid attack). Taken together, these results suggest that the aphids can either invest in defence (parasitoid resistance, increased off-plant survival time) or reproduction, and speculate that this may be mediated by changes in the aphids' endosymbiont fauna. Furthermore, there is a positive relationship between aphid size and resistance, suggesting that successful resistance to parasitoid attack may involve physical, as well as physiological, defences.

Costs of resistance in insect-parasite and insect-parasitoid interactions.

Most, if not all, organisms face attack by natural enemies and will be selected to evolve some form of defence. Resistance may have costs as well as its obvious benefits. These costs may be associated with actual defence or with the maintenance of the defensive machinery irrespective of whether a challenge occurs. In this paper, the evidence for costs of resistance in insect-parasite and insect-parasitoid systems is reviewed, with emphasis on two host-parasitoid systems, based on Drosophila melanogaster and pea aphids as hosts. Data from true insect-parasite systems mainly concern the costs of actual defence; evidence for the costs of standing defences is mostly circumstantial. In pea aphids, the costs of standing defences have so far proved elusive. Resistance amongst clones is not correlated with life-time fecundity, whether measured on good or poor quality plants. Successful defence by a D. melanogaster larva results in a reduction in adult size and fecundity and an increased susceptibility to pupal parasitoids. Costs of standing defences are a reduction in larval competitive ability though these costs only become important when food is limited. It is concluded that costs of resistance can play a pivotal role in the evolutionary and population dynamic interactions between hosts and their parasites.