Density-dependent intraguild predation of an aphid parasitoid

A growing body of research has examined the effect of shared resource density on intraguild predation (IGP) over relatively short time frames. Most of this work has led to the conclusion that when the shared resource density is high, the strength of IGP should be lower, due to prey dilution. However, experiments addressing this topic have been done using micro- or mesocosms that excluded the possibility of intraguild predator aggregation. We examined the effect of shared resource density on IGP of an aphid parasitoid in an open field setting where the effects of prey dilution and predator aggregation could occur simultaneously. We brought potted soybean plants with 2, 20, or 200 soybean aphids (Aphis glycines) and 20 pupae (‘mummies’) of the soybean aphid parasitoid Binodoxys communis into soybean fields in Minnesota, USA. We monitored predator aggregation onto the potted plants, predation of parasitoid mummies, and successful adult emergence of B. communis. We found that predator aggregation was higher at the higher aphid densities on our experimental plants and that this coincided with lower adult emergence of B. communis, indicating that even if a prey dilution effect occurred in our study, it was overcome by short-term predator aggregation. Our results suggest that the effect of shared resource density on IGP may be more nuanced in a field setting than in microcosms due to predator aggregation.     

Multifaceted determinants of host specificity in an aphid parasitoid

The host specificity of insect parasitoids and herbivores is thought to be shaped by a suite of traits that mediate host acceptance and host suitability. We conducted laboratory experiments to identify mechanisms shaping the host specificity of the aphid parasitoid Binodoxys communis. Twenty species of aphids were exposed to B. communis females in microcosms, and detailed observations and rearing studies of 15 of these species were done to determine whether patterns of host use resulted from variation in factors such as host acceptance or variation in host suitability. Six species of aphids exposed to B. communis showed no signs of parasitism. Four of these species were not recognized as hosts and two effectively defended themselves from attack by B. communis. Other aphid species into which parasitoids laid eggs had low suitability as hosts. Parasitoid mortality occurred in the egg or early larval stages for some of these hosts but for others it occurred in late larval stages. Two hypotheses explaining low suitability were investigated in separate experiments: the presence of endosymbiotic bacteria conferring resistance to parasitoids, and aphids feeding on toxic plants. An association between resistance and endosymbiont infection was found in one species (Aphis craccivora), and evidence for the toxic plant hypothesis was found for the milkweed aphids Aphis asclepiadis and Aphis nerii. This research highlights the multifaceted nature of factors determining host specificity in parasitoids.     

An inherited virus influences the coexistence of parasitoid species through behaviour manipulation

The potential role of pathogens or parasites in maintaining species coexistence is well documented. However, the impact of vertically transmitted symbionts, that can markedly modify their host's biology, is largely unknown. Some females of the Drosophila parasitoid Leptopilina boulardi are infected with an inherited virus (LbFV). The virus forces females to lay supernumerary eggs in already parasitised hosts, thus allowing its horizontal transmission. Using two independent experimental procedures, we found that LbFV impacts inter-specific competition between L. boulardi and the related L. heterotoma. While L. boulardi rapidly outcompetes L. heterotoma in the absence of the virus, L. heterotoma was able to maintain or even to eliminate L. boulardi in the presence of LbFV. By forcing females to superparasitise, LbFV induced egg wastage in L. boulardi thus explaining its impact on the competition outcome. We conclude that this symbiont whose transmission is L. boulardi-density-dependant may affect the coexistence of Leptopilina species.     

Influence of wheat and oat cultivars on the development of the cereal aphid parasitoid Aphidius rhopalosiphi and the generalist aphid parasitoid Ephedrus plagiator

The effects of three wheat cultivars and two oat cultivars on the development of the cereal aphid parasitoid Aphidius rhopalosiphi De Steph. and the generalist aphid parasitoid Ephedrus plagiator (Nees) (Hymenoptera: Braconidae) were evaluated in the laboratory. The level of hydroxamic acids, a family of secondary metabolites that can affect the mean relative growth rate of cereal aphids in cereals, were measured in the different cultivars. The parasitoids were reared in Sitobion avenae (F.) (Homoptera: Aphididae), using plants grown under greenhouse conditions. A. rhopalosiphi showed a longer developmental time on wheat relative to oat cultivars. This effect was accounted for by a significant increase in the time from oviposition to pupation (mummy formation), while the duration of the pupal stage remained constant between treatments. No further effects were observed in other variables evaluating A. rhopalosiphi performance, such as adult longevity, adult body weight and secondary sex ratio. The generalist E. plagiator did not show significant differences in any of the variables analysed, both between cultivars and cereal species. Hydroxamic acids levels correlated negatively with mean relative growth rates of S. avenae, but positively with the observed developmental time of A. rhopalosiphi. The results are discussed in terms of tritrophic effects and the development of breeding programmes trying to improve plant resistance to aphids.     

Host range limitation caused by incomplete host regulation in an aphid parasitoid

Defining host ranges in parasitoid insects is important both from a theoretical and an applied point of view. Based on the literature, some species seem able to use a wide range of hosts, while field studies indicate possible local host specialization. In koinobiont endoparasitoid species, such specialization could involve physiological processes. We tested the ability of two strains of the cosmopolitan and polyphagous parasitoid Diaeretiella rapae, to develop in three of its recorded aphid host species. Both strains produced high parasitism rates on the cabbage aphid Brevicoryne brassicae and the green peach aphid Myzus persicae but almost no progeny on the cherry-oat aphid Rhopalosiphum padi. This last species was less attacked by female parasitoids. Moreover, parasitoid eggs and larvae were smaller than in the two other host aphid species and their development was delayed. This abnormal development appeared to be due to an incomplete host regulation process, probably related to the low number and the size of teratocytes produced by D. rapae in R. padi individuals. Such a failure as far as gaining control of the host's metabolism is concerned could play an important role in shaping the host range of parasitoid insects, leading to local variation of the host spectrum in populations from various geographical areas.     

Effects of intraguild predation on aphid parasitoid survival

To assess the potential selection pressure caused by intraguild predation between predators and parasitoids of aphids an estimate was made of the predation risk to Aphis fabaeScop. mummified by Lysiphlebus fabarum(Marshall, 1896) on sugar beet. Mummified aphids were exposed to a natural community of predators. Their survival time was estimated during a 10-day field survey. Additionallythe role of alternative prey on parasitoid survival was investigated by adding unparasitised aphids to half of the mummy aggregations.The field data were evaluated by survival analysis. Two covariates were tested within a Cox proportional hazard model: (i) the presence of the alternative prey and (ii) the patch structure (number of proximal mummies attacked). Within 4–5 days after exposure predators destroyed approx. 50% of the mummies. The model with both covariates revealed a significant difference concerning survival of the mummies in the two treatments (Likelihood ratio test, ²=78.03, P=0.0001). Alternative prey reduced the predation risk on mummies by 29%, while a high level of predation on proximal mummies increased the individual predation risk by 4%. The results are discussed in the context of prey location by predators and the evolution of anti-predator mechanisms.     

烟蚜茧蜂对蚜虫信息素及烟草挥发物的触角电位反应

利用触角电位(EAG)技术测定了烟蚜茧蜂(Aphididius gifuensis)对蚜虫性信息素(荆芥醇和荆芥内酯)和报警信息素(反-β-法尼烯)以及烟草挥发性物质的电生理反应.结果表明:雌蜂和雄蜂对蚜虫性信息素、报警信息素、烟草挥发物均有反应,但雌雄蜂对这些化学信息物质的嗅觉敏感性存在差异,雌蜂对荆芥醇、荆芥内酯、顺-3-己烯-1-醇、反-2-己烯醛、水杨酸甲酯和里那醇的EAG反应都大于雄峰,证明雌雄蜂在利用寄主栖境中信息化学物质方面存在不同的策略,它们分别识别了不同的有关寄主的化学指纹图;烟蚜茧蜂对烟草气味组分具有不同的敏感性,对绿叶气味组分的EAG反应要强于对萜类化合物的反应,绿叶气味组分很有可能在其寻找桃蚜的过程中发挥远距离定向作用.     

Impact of the entomopathogenic fungus Verticillium lecanii on development of an aphid parasitoid, Aphidius colemani

The parasitoid Aphidius colemani developed normally (approximately 90% adult emergence) when its cotton aphid (Aphis gossypii) host was treated with Verticillum lecanii conidia 5 or 7 days after parasitization. Fungus exposure 1 day before or up to 3 days after parasitization, however, reduced A. colemani emergence from 0 to 10%. Also, numbers of spores and mycelial fragments in aphid homogenates were much higher in aphids exposed to the fungus up to 3 days after parasitization than in aphids treated after 5 or 7 days. Our results suggest that the parasitoid and fungus may be used together for aphid biocontrol as long as fungus applications are timed to allow late-instar development of the parasitoid.     

Host size induced variation in progeny sex ratio of an aphid parasitoid Lysiphlebia mirzai

A study aimed at determining the effect of host size on the pattern of sex allocation by an aphid parasitoid Lysiphlebia mirzai Shuja-Uddin (Hymenoptera: Braconidae: Aphidiinae) was undertaken to test the validity of the following three hypotheses: (1) larger hosts will yield a greater proportion of daughters, (2) differential mortality of the sexes of the parasitoid during development is a function of host-size, and (3) daughters emerging from larger hosts are more fecund. The results suggested a propensity in the parasitoid to deposit fertilised (diploid) eggs in large hosts (third instar nymph) and unfertilised (haploid) eggs in small hosts (first and second instar nymphs). Unpreferred fourth instar nymphs and apterous aphid adults also received more haploid eggs despite being larger in size than the preferred third instar nymphs. However, the perception of host size by the mother was dependent on the extent of temporal variation in the host size distribution and on her previous experience of host size. Developmental period, longevity, mating potential, fecundity and progeny sex ratio of L. mirzai emerging from small versus large hosts indicated that the host size affected the fitness of the daughters more than that of sons. No differential mortality of the sexes during development of L. mirzai was observed in small versus large hosts. This shows that L. mirzai, while ovipositing in growing stages of the host, adjusts progeny sex ratio according to the host size and by doing so she tends to contribute maximally to progeny fitness without knowing about the future host quality.     

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.     

The performance of an aphid parasitoid is negatively affected by the presence of a circulative plant virus

Plant viruses and aphids can interact via contest competition for plant resources and induce changes in plant physiology, which can have effects on a third trophic level. The aim of this study was to determine how the interactions between a circulative plant virus and its aphid vector may affect the performance of an endoparasitoid and how parasitism may affect the efficiency of virus transmission by its aphid vector. The timing when parasitized aphids were transferred to virus-infected lettuce leaves was critical for the performance of A. ervi. Higher parasitoid larvae mortality, longer developmental times and lower percentages of mummification were detected on viruliferous/parasitized aphid nymphs when the time lag between parasitism and exposure to the virus was less than 24 h. No significant differences were detected in virus transmission rate between parasitized and non-parasitized M. euphorbiae aphids.     

The effects of two species of hymenopterous parasitoid on the reproductive system of the pea aphid, Acyrthosiphon pisum

Two cultures of first instar pea aphids, Acyrthosiphon pisum (Harris) (Homoptera: Aphididae), were subjected to parasitization by Ephedrus plagiator (Nees) and Aphidius ervi Haliday (Hymenoptera: Braconidae) respectively, and a third culture, of fourth instar pea aphids, was subjected to parasitization by E. plagiator. Significant parasitogenic effects on the reproductive system occurred within 24 h of exposure to parasitoids in the form of reductions in both embryo number and the size of the largest embryo, and degenerative changes in the embryos themselves. No evidence was found of direct feeding by the larvae on the host's tissues, until just before larval pupation. The largest embryos of some fourth instar aphids escaped the effects of parasitization probably because they had developed a resistant cuticle by the time of oviposition by the parasitoid. Results suggested that embryonic degeneration was an indirect effect of parasitization due to starvation, interference with the aphid's hormone levels, or both.

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Résumé Trois élevages de 100 à 200 premiers stades d'A. pisum, nés à 24 heures les uns des autres, ont été divisés chacun en un lot témoin et un lot expérimental. Deux des élevages expérimentaux ont alors été soumis au parasitisme d'Ephedrus plagiator ou de Aphidius ervi, le troisième élevage a pu se développer jusqu'au 4è stade avant d'être exposé à E. plagiator. Des échantillons de 10 pucerons ont été retirés de chaque lot après 24 heures et ensuite toutes les 48 heures pour être disséqués dans du liquide physiologique. Les nombres d'ovarioles et d'embryons et la taille du plus gros embryon ont été notés. Des cellules développées, issue de la séreuse de l'oeuf de l'hyménoptère se sont disséminées dans l'hémolymphe de l'hôte et ont servi d'aliment aux larves en développement. Seul le dernier stade larvaire des parasitoïdes s'est alimenté sur les tissus de l'hôte et ceci avait lieu juste avant la nymphose. Des effets significatifs se sont traduits après 24 heures par la réduction du nombre des embryons, par la diminution de la taille du plus grand de ceux-ci et par des altérations dans les embryons eux-mêmes.

     

Fungal endosymbionts of plants reduce lifespan of an aphid secondary parasitoid and influence host selection

Complex biotic interactions shape ecological communities of plants, herbivores and their natural enemies. In studies of multi-trophic interactions, the presence of small, invisible micro-organisms associated with plants and those of a fourth above-ground trophic level have often been neglected. Incorporating these neglected factors improves our understanding of the processes within a multi-trophic network. Here, we ask whether the presence of a fungal endosymbiont, which alters plant quality by producing herbivore-toxic substances, trickles up the food chain and affects the performance and host-selection behaviour of aphid secondary parasitoids. We simultaneously offered hosts from endophyte-free and endophyte-infected environments to secondary parasitoids. Older and more experienced parasitoid females discriminated against hosts from the endophyte-infected environment. Developing in lower quality hosts from the endophyte-infected environment reduced the lifespan of secondary parasitoids. This indicates that aphid secondary parasitoids can perceive the disadvantage for their developing offspring in parasitoids from the endophyte environment and can learn to discriminate against them. In the field, this discrimination ability may shift the success of primary parasitoids to endophyte-infected plants, which co-occur with endophyte-free plants. Ultimately, the control of aphids depends on complex interactions between primary and secondary parasitoids and their relative sensitivity to endophytic fungi.     

The use of kairomones for foraging decisions by an aphid parasitoid in small host aggregations

1. The wasp Diaeretiella rapae uses honeydew emitted by its host, the cabbage aphid Brevicoryne brassica, as a kairomone (chemicals emitted by an organism as part of its activity and used by its natural enemies to their advantage). The role of the kairomone in foraging decisions by the parasitic wasp was explored by manipulating the amount of honeydew and the number of aphids in a colony independently. The count-down patch-exploitation mechanism (Iwasa et al., 1981) was employed to predict the results of these manipulations and contrast them with the predictions of Waage's (1979) model. 2. Kairomonal activity of honeydew decreased as the honeydew aged and lost its activity completely within 72 h. 3. The wasp was exposed to different amounts of honeydew on (a) aphid-free leaves and (b) leaves bearing colonies of 150 aphids. The parasitoid search time on both leaf types increased with increasing honeydew contamination. On aphid-bearing leaves, the number of attacked aphids in the colonies also increased with increasing honeydew contamination. The presence of aphids reduced the parasitoid search time compared to search time on aphid-bearing leaves with the same level of honeydew contamination, as predicted by the count-down model. 4. Parasitoids exposed to the same amount of honeydew, but a different number of aphids in a colony on the leaf, first increased the number of aphids attacked in relation to the number of aphids in the colony. But as the colony reached a certain size, the number of aphids attacked levelled off, despite the increase in the number of aphids in the colony. Search time was variable but did not exhibit any trend as the number of aphids in the colonies increased. 5. These results suggest that honeydew level is used by D. rapae as a cue for assessment of the number of aphids in the colony. In such cases, a count-down exploitation mechanism gives the best results to a forager. Many parasitoids may use kairomones for patch assessment and will therefore employ a count-down rule during patch exploitation.     

Foraging by the aphid parasitoid Ephedrus cerasicola for patchily distributed hosts

Females of the aphid parasitoid Ephedrus cerasicola were released into small glasshouses containing 20–25 paprika plants (Capsicum annuum L.), either aphid-free (controls) or infested with different numbers of Myzus persicae (Sulzer), i.e. from 0 to about 1000 aphids per plant. The number of parasitoids per plant were counted 1 h, 2 h, 3 h, 4 h, 5 h, 6 h, 8 h and about 24 h after the release. During the last inspection (24 h) the parasitoids were removed. In the aphid-infested houses, the parasitoids soon gathered on the most heavily infested plants (500–1000 aphids per plant), while the aphid-free and low-infested plants (50–200 aphids per plant) were almost free from parasitoids. In the aphid-free houses, a significantly lower portion of the released parasitoids were found on the plants, and they did not show any preference for certain plants. The percentage parasitism, based on mummies on the plants, was rather density independent after a slight peak on plants with about 50 aphids. No superparasitism was found by dissection of aphids.

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Résumé Des femelles de l'aphidophage Ephedrus cerasicola ont été lachées dans de petites serres contenant 20 à 25 pieds de paprika (Capsicum annuum), contaminés par des effectifs de 0 (témoins) à 1000 pucerons (Myzus persicae) par pied. Le nombre de parasitoïdes par plante a été rélevé 1 h, 2 h, 3 h, 4 h, 5 h, 6 h, 8 h, et environ 24 h après leur libération. Les E. cerasicola adultes ont été retirés lors de la dernière inspection (24 h). Dans les serres infestées, les femelles se rassemblent sur les plantes les plus contaminées (500 à 1000 pucerons par pied), tandis que les plantes sans pucerons ou faiblement contaminées (50 à 200 par plante) n'en avaient presque pas. Dans les serres sans pucerons, des femelles en proportion significativement plus faible ont été trouvées sur les plantes, sans qu'elles aient manifesté une préférence pour certaines d'entre elles. Le taux de parasitisme, d'après le nombre de momies par plante, est apparu plutôt indépendant de la densité, après un faible pic pour les plantes avec environ 50 pucerons. Les dissections de pucerons n'ont révélé aucun superparasitisme.

     

Temperature effects during development on a polyembryonic parasitoid and its host

Ambient temperature can influence development through effects on metabolic rate and by inducing physiological stress. In this study, we assessed temperature effects on a host–parasitoid interaction and on the body size and brood size of emerging wasps. By examining the development at two different temperatures of the koinobiont parasitoid, Copidosoma bakeri, and its host, Agrotis ipsilon, we asked: (1) Does the growth response to temperature by A. ipsilon depend on whether the moth caterpillar is parasitized? (2) Does the allocation pattern of body size and brood size in C. bakeri change with temperature? To answer these questions, we exposed A. ipsilon larvae parasitized by C. bakeri to high or low non-lethal temperatures when A. ipsilon was in early or late larval stages and measured their development time and body mass for all four treatment combinations. We also examined the brood size and body mass of emerging wasps. Whether parasitized or not, A. ipsilon larvae decreased development time, but generally did not decrease final body mass, at the higher temperature. When parasitized A. ipsilon was exposed to the higher temperature only late in their development, enlargement of the host by the parasitoid was reduced. C. bakeri brood size significantly increased when the higher temperature was applied early in host development. We did not detect a shift with temperature in the allocation pattern of the size–number trade-off for wasp offspring, suggesting that this trade-off relationship may be under selection strong enough to yield insensitivity to temperature.     

Lysiphlebus testaceipes,an introduced aphid parasitoid in portugal [Hym.: Aphidiidae]

Lysiphlebus testaceipes (Cresson), an exotic parasitoid species introduced in 1973–74 into southern France and subsequently widespread over the whole mediterranean France, Italy and Spain has become established even in Portugal since 1985. It was found on the southern coast of Portugal parasitizingAphis nerii Boyer de Fonscolombe. In 1986 it spread towards the North, its host range expanded and now includesAphis chloris Koch,Aphis citricola van der Goot,Aphis fabae Scopoli,Aphis frangulae Kaltenbach,Aphis gossypii Glover,A. nerii, Aphis parietariae Theobald,Aphis sedi Kaltenbach,Toxoptera aurantii (Boyer de Fonscolombe). The proved complete development and a high parasitization ofL. testaceipes onA. citricola is the 1st case in the whole Mediterranean, from where only incomplete development and a negligible percentage of parasitization (Italy) have been reported. Both the host range composition and development ofL. testaceipes indicate an increase of genetic polymorphism in the established populations. Interspecific relations ofL. testaceipes and the indigenous parasitoid species indicate an increasing dominance of the exotic biocontrol agent.      

Glucosinolate genetics and the attraction of the aphid parasitoid Diaeretiella rapae to Brassica

The control of insect pests using parasitoids and carnivores has been successfully applied in protected cropping systems, orchards and forestry. Their success in annual field crops has been more limited due largely to the difficulties of attracting and maintaining a sufficient density of parasitoids in the crop before the levls of the insect herbivores become economically damaging. Parasitoids are known to be attracted to host-plant volatiles; thus, manipulating the host-plant chemistry may provide a means of enhancing the attraction of parasitoids to their prey. In this study we describe the differential attraction of the braconid wasp Diaeretiella rapae to two near-isogenic lines of Brassica oleracea which differ in a gene which alters the chemical structure of the isothiocyanates which are emitted following tissue damage. We demonstrate that, by enhancing the production of but-3-enyl isothiocyanate in B. oleracea and Brassica napus (oilseed rape), we can increase the attraction of D. rapae to these plants under standard field conditions.     

Metabolic and proteomic profiling of diapause in the aphid parasitoid Praon volucre

Background

Diapause, a condition of developmental arrest and metabolic depression exhibited by a wide range of animals is accompanied by complex physiological and biochemical changes that generally enhance environmental stress tolerance and synchronize reproduction. Even though some aspects of diapause have been well characterized, very little is known about the full range of molecular and biochemical modifications underlying diapause in non-model organisms.

Methodology/Principal Findings

In this study we focused on the parasitic wasp, Praon volucre that exhibits a pupal diapause in response to environmental signals. System-wide metabolic changes occurring during diapause were investigated using GC-MS metabolic fingerprinting. Moreover, proteomic changes were studied in diapausing versus non-diapausing phenotypes using a combination of two-dimensional differential gel electrophoresis (2D-DIGE) and mass spectrometry. We found a reduction of Krebs cycle intermediates which most likely resulted from the metabolic depression. Glycolysis was galvanized, probably to favor polyols biosynthesis. Diapausing parasitoids accumulated high levels of cryoprotective polyols, especially sorbitol. A large set of proteins were modulated during diapause and these were involved in various functions such as remodeling of cytoskeleton and cuticle, stress tolerance, protein turnover, lipid metabolism and various metabolic enzymes.

Conclusions/Significance

The results presented here provide some first clues about the molecular and biochemical events that characterize the diapause syndrome in aphid parasitoids. These data are useful for probing potential commonality of parasitoids diapause with other taxa and they will help creating a general understanding of diapause underpinnings and a background for future interpretations.