Female Parasitic Wasps Research Articles

Comparative transcriptome and proteome reveal the unique genes and proteins of female parasitic wasps, Lysiphlebia japonica Ashmead.

Lysiphlebia japonica Ashmead (Hymenoptera, Braconidae) is an endophagous parasitoid wasp and its host, Aphis gossypii Glover (Hemiptera, Aphididae) is a major cotton pest. L. japonica affects the growth and fatty acid metabolism of cotton aphids after parasitization and has been widely used as a biocontrol agent. However, there are currently few reports about the molecular characteristics of L. japonica, especially the differences between male and female. In this study, using transcriptome and proteome analysis of the abdomen of female and male parasitic wasps, respectively, we obtained a total of 27,169 DEGs and 1,194 DEPs, then a total of 909 positively correlated high-expression proteins and genes were obtained by combined omics analysis. Subsequently, 20 differentially expressed abdomen specific proteins were selected for validation by RT-qPCR and Multiple Reaction Monitoring (MRM) protein verification. The result of RT-qPCR demonstrated that all 20 genes were highly expressed in the abdomen of females, and five target proteins with unique peptide fragments and identification profiles were identified by MRM, which were venom protease, tropomyosin, lipase member I, venom serine carboxypeptidase and calreticulin, respectively. Overall, these results provided molecular resources for the differences between males and females in L. japonica and the screened 20 abdomen specific proteins were verified to demonstrate the validity of the data, which offered important molecular data resources for further studies on the related functional genes of parasitic wasps and the mechanism of parasitoids regulating the growth of aphids. © 2023 Society of Chemical Industry.

Food or host: do physiological state and flower type affect foraging decisions of parasitoids?

Within the optimal foraging theory framework, parasitoids constitute ideal models to elucidate combined physiological and environmental determinism of foraging behavior between current and future fitness gains. Parasitoid females need hosts to lay eggs for their reproduction (immediate gain), but also sugar food resources for their survival (future gain). According to theoretical models and previous empirical studies, fed females should favor host foraging, whereas females with lower energetic reserves should search for food. Surprisingly, the influence of mating status and food quality has not been considered, whereas they may both constitute major factors altering animals’ choices between reproducing and feeding. We tested decision-making on Aphidius rhopalosiphi parasitoid females with different life expectancy levels (as set by recent feeding history) and mating status, using two flower species with contrasted attractiveness and nectar suitability. Interestingly, all fed and unfed females with different expected lifetime levels favored reproduction over nutrition since they are mated. This could be explained by their reproductive status that appeared to be the main determinant of their foraging decisions. For a given expected lifetime, mated females favored more reproduction whereas unmated ones favored food. Physiological status of females (mating and lifetime expectancy) did not interact with flower species on their foraging decisions nor did it modify their preferences, as they always favored the most attractive flower, which does not have the best nectar. These results highlight the need for more empirical studies to evaluate the interactions between different intrinsic factors and to carefully consider the mating status in model assumptions, as it influences foraging behavior between immediate and future fitness gains. Parasitic wasps need hosts to lay eggs for their reproduction (immediate fitness gain) and sugar resources for their survival (future fitness gain). Empirical studies and related theoretical models about foraging decisions of parasitic wasps between current and future gains included influences of energetic and resource availability constrains. We examined assumptions used by those mathematical models by empirically testing two new factors, food qualities provided by two nectar provisioning flower species with contrasted functional traits, which had surprisingly no impact on decision-making, and mating status which we showed to play a decisive role on decision-making between food or host resources. These factors should henceforth be considered in model assumptions or in models themselves to realize accurate predictions and to provide a better understanding of foraging decisions made by female parasitic wasps.

Mechanisms of ovipositor insertion and steering of a parasitic wasp

Drilling into solid substrates with slender beam-like structures is a mechanical challenge, but is regularly done by female parasitic wasps. The wasp inserts her ovipositor into solid substrates to deposit eggs in hosts, and even seems capable of steering the ovipositor while drilling. The ovipositor generally consists of three longitudinally connected valves that can slide along each other. Alternative valve movements have been hypothesized to be involved in ovipositor damage avoidance and steering during drilling. However, none of the hypotheses have been tested in vivo. We used 3D and 2D motion analysis to quantify the probing behavior of the fruit-fly parasitoid Diachasmimorpha longicaudata (Braconidae) at the levels of the ovipositor and its individual valves. We show that the wasps can steer and curve their ovipositors in any direction relative to their body axis. In a soft substrate, the ovipositors can be inserted without reciprocal motion of the valves. In a stiff substrate, such motions were always observed. This is in agreement with the damage avoidance hypothesis of insertion, as they presumably limit the overall net pushing force. Steering can be achieved by varying the asymmetry of the distal part of the ovipositor by protracting one valve set with respect to the other. Tip asymmetry is enhanced by curving of ventral elements in the absence of an opposing force, possibly due to pretension. Our findings deepen the knowledge of the functioning and evolution of the ovipositor in hymenopterans and may help to improve man-made steerable probes.

Combined use of herbivore‐induced plant volatiles and sex pheromones for mate location in braconid parasitoids

Herbivore-induced plant volatiles (HIPVs) are important cues for female parasitic wasps to find hosts. Here, we investigated the possibility that HIPVs may also serve parasitoids as cues to locate mates. To test this, the odour preferences of four braconid wasps - the gregarious parasitoid Cotesia glomerata (L.) and the solitary parasitoids Cotesia marginiventris (Cresson), Microplitis rufiventris Kokujev and Microplitis mediator (Haliday) - were studied in olfactometers. Each species showed attraction to pheromones but in somewhat different ways. Males of the two Cotesia species were attracted to virgin females, whereas females of M. rufiventris were attracted to virgin males. Male and female M. mediator exhibited attraction to both sexes. Importantly, female and male wasps of all four species were strongly attracted by HIPVs, independent of mating status. In most cases, male wasps were also attracted to intact plants. The wasps preferred the combination of HIPVs and pheromones over plant odours alone, except M. mediator, which appears to mainly use HIPVs for mate location. We discuss the ecological contexts in which the combined use of pheromones and HIPVs by parasitoids can be expected. To our knowledge, this is the first study to show that braconid parasitoids use HIPVs and pheromones in combination to locate mates.

Female‐biased sex ratio shifts in a solitary parasitoid and their effects on virginity, population dynamics, and biological control

AbstractMated female parasitic wasps can control the sex of their offspring by controlling which eggs are exposed to sperm. Females that have failed to mate, however, are restricted to producing only male offspring, as all their eggs are unfertilized. We incorporated the effects of these sometimes constrained, sometimes flexible parasitoid sex ratios into a basic Nicholson–Bailey population model. We found that the less common case of an increasing female bias in response to competition can destabilize dynamics and have both positive and negative effects on host suppression. We also incorporated the effects of virginity due to a lack of males into the model. Virginity had stabilizing effects on parasitoid‐host population dynamics, and prevented runaway female bias in a parasitoid population. We found that the changes in host suppression caused by these new behaviours can be either positive or negative, and are highly dependent on the search efficiency of the parasitoid.

Ecdysteroid receptor docking suggests that dibenzoylhydrazine‐based insecticides are devoid of any deleterious effect on the parasitic wasp Psyttalia concolor (Hym. Braconidae)

The moulting accelerating compounds (MACs) or ecdysteroid agonists represent a selective group of insecticides acting upon binding to the ecdysteroid receptor (EcR) and leading to lethal premature moulting in larval stages and aborted reproduction in adults. Psyttalia concolor Szèpl. is a useful parasitic wasp attacking important tephritid pests such as the medfly and olive fruit fly. Contact and oral exposure in the laboratory of female parasitic wasps to the dibenzoylhydrazine-based methoxyfenozide, tebufenozide and RH-5849 did not provoke negative effects. No mortality and no reduction in beneficial capacity were observed. The ligand-binding domain (LBD) of the EcR of P. concolor was sequenced, and a homology protein model was constructed which confirmed a cavity structure with 12 α-helices, harbouring the natural insect moulting hormone 20-hydroxyecdysone. However, a steric clash occurred for the MAC insecticides owing to a restricted extent of the ligand-binding cavity of the PcLBD-EcR, while they did dock well in that of susceptible insects. The insect toxicity assays demonstrated that MACs are selective for P. concolor. The modelling/docking experiments are indications that these insecticides do not bind with the LBD-EcR of P. concolor and support the theory that they show no biological effects in the parasitic wasp. These data may help in explaining the compatible use of MACs together with parasitic wasps in IPM programmes.

Chemical Ecology of Egg Parasitoids Associated with True Bugs

Parasitoids representing some 15 families of Hymenoptera develop in insect eggs; three of these families, Platygastridae (= Scelionidae), Mymaridae, and Encyrtidae, are associated with Heteroptera. Several species of heteropteran egg parasitoids are or may be important for biological pest control. Successful parasitism of insect herbivores by insect parasitoids arises through several phases of host searching, which lead female wasps to the vicinity of, or in contact with, their hosts. During the host location process, females encounter and explore a variety of stimuli, among which chemical cues (i.e., semiochemicals or infochemicals) play a pivotal role. Female parasitoids are under selection pressure to efficiently invest their limited time on the location and exploitation of host-derived stimuli. In general, the levels of reliability and detectability of a particular stimulus are inversely correlated. Female parasitic wasps adopt differing strategies to solve this dilemma. In this paper we focus on the various host selection strategies employed by heteropteran egg parasitoids and possible means whereby the chemically mediated behavior of these wasps may be exploited to enhance biological pest control.

A hitchhiker’s guide to a crowded syconium: how do fig nematodes find the right ride?

Summary 1. Organisms with low mobility, living within ephemeral environments, need to find vehicles that can disperse them reliably to new environments. The requirement for specificity in this passenger–vehicle relationship is enhanced within a tritrophic interaction when the environment of passenger and vehicle is provided by a third organism. Such relationships pose many interesting questions about specificity within a tritrophic framework. 2. Central to understanding how these tritrophic systems have evolved, is knowing how they function now. Determining the proximal cues and sensory modalities used by passengers to find vehicles and to discriminate between reliable and non‐reliable vehicles is, therefore, essential to this investigation. 3. The ancient, co‐evolved and highly species‐specific nursery pollination mutualism between figs and fig wasps is host to species‐specific plant‐parasitic nematodes which use fig wasps to travel between figs. Since individual globular fig inflorescences, i.e. syconia, serve as incubators for hundreds of developing pollinating and parasitic wasps, a dispersal‐stage nematode within such a chemically complex and physically crowded environment is faced with the dilemma of choosing the right vehicle for dispersal into a new fig. Such a system therefore affords excellent opportunities to investigate mechanisms that contribute to the evolution of specificity between the passenger and the vehicle. 4. In this study of fig–wasp–nematode tritrophic interactions in Ficus racemosa within which seven wasp species can breed, we demonstrate using two‐choice as well as cafeteria assays that plant‐parasitic nematodes (Schistonchus racemosa) do not hitch rides randomly on available eclosing wasps within the fig syconium, but are specifically attracted, at close range, i.e. 3 mm distance, to only that vehicle which can quickly, within a few hours, reliably transfer it to another fig. This vehicle is the female pollinating wasp. Male wasps and female parasitic wasps are inappropriate vehicles since the former are wingless and die within the fig, while the latter never enter another fig. Nematodes distinguished between female pollinating wasps and other female parasitic wasps using volatiles and cuticular hydrocarbons. Nematodes could not distinguish between cuticular hydrocarbons of male and female pollinators but used other cues, such as volatiles, at close range, to find female pollinating wasps with which they have probably had a long history of chemical adaptation. 5. This study opens up new questions and hypotheses about the evolution and maintenance of specificity in fig–wasp–nematode tritrophic interactions.

Foraging behavior of egg parasitoids exploiting chemical information

Female parasitic wasps seek hosts for their offspring often in a dynamic environment. Foraging egg parasitoids rely on a variety of chemical cues originating from the adult host, host products, or the host plant rather than from the attacked host stage?the insect egg itself. Besides pupae, insect eggs are the most inconspicuous host stage attacked by parasitic wasps. To overcome the problem of low detectability of host eggs, egg parasitoids have evolved several strategies such as exploiting long-range kairomones of the adult hosts, for example, host aggregation and sex pheromones, plant synomones induced by egg deposition or host feeding, or short-range contact cues derived from the adult host or the host plant. Moreover, egg parasitoids have evolved the ability to use chemical espionage in combination with hitchhiking on the adult host (phoresy) to compensate their limited flight capability and to gain access to freshly laid host eggs. Here, we provide a comprehensive overview on the variety of host-foraging strategies of egg parasitoids exploiting chemical signals. Furthermore, the use of such infochemicals is discussed with respect to the wasps? dietary breadth and their ability to learn

Comparison of detection ability of learned odors between males and females in the larval parasitoid Microplitis croceipes

AbstractAlthough female parasitic wasps are known to learn to associate odors with hosts and food, the ability of males to learn and detect odors has been neglected. We conducted laboratory experiments to compare the detection ability of learned odors between males and females in the larval parasitoid Microplitis croceipes (Cresson) (Hymenoptera: Braconidae). We first conditioned males and females to associate sucrose water with methyl benzoate, 3‐octanone, or cyclohexanone, and then observed their behavior toward various concentrations (40 ng l−1−4 mg l−1) of the trained odors. Conditioned male wasps responded as well as female wasps to various concentrations of the three odors. Response times by wasps to these three odors were not significantly different between sexes. For the three odors, response times of both sexes were longer at the intermediate concentrations (40–400 µg l−1) than the higher or lower concentrations. The present study suggests that M. croceipes males can learn and respond to the three chemicals tested as well as the females, and conditioned males are as sensitive to learned odors as conditioned females. By using their sensitive learning and odor‐detection capabilities, M. croceipes males could search for food sources as efficiently as females under natural conditions.

A Plasma Membrane Protein from Zea mays Binds with the Herbivore Elicitor Volicitin

Volicitin (17-hydroxylinolenoyl-l-Gln) present in the regurgitant of Spodoptera exigua (beet armyworm caterpillars) activates the emission of volatile organic compounds (VOCs) when in contact with damaged Zea mays cv Delprim (maize) leaves. VOC emissions in turn serve as a signaling defense for the plant by attracting female parasitic wasps that prey on herbivore larvae. A tritiated form of volicitin was synthesized and shown to induce volatiles in the same fashion as the biological form. [(3)H]-l-volicitin rapidly, reversibly, and saturably bound to enriched plasma membrane fractions isolated from Z. mays leaves with an apparent K(d) of 1.3 nM and a Hill coefficient of 1.07. Analog studies showed that the l-Gln and hydroxy moieties of volicitin play an important role in binding. Treatment of plants with methyl jasmonate (MeJA) increased the total binding of [(3)H]-l-volicitin to the enriched plasma membrane more than threefold, suggesting that MeJA activates transcription of the gene encoding the binding protein. S. exigua feeding also increased total binding fourfold. Cycloheximide pretreatment of plants significantly decreased binding of radiolabeled volicitin to the enriched plasma membrane. These data provide the first experimental evidence that initiation of plant defenses in response to herbivore damage can be mediated by a binding protein-ligand interaction.

In situ translocation of volicitin by beet armyworm larvae to maize and systemic immobility of the herbivore elicitor in planta.

Volicitin (N-[17-hydroxylinolenoyl]-L glutamine) present in the regurgitant of beet armyworm (Spodoptera exigua) activates the emissions of volatile organic compounds (VOCs) when in contact with damaged corn (Zea mays L.) leaves. VOC emission in turn serves as a signaling defense for the plant by attracting female parasitic wasps that prey on herbivore larvae. Chemical tracking of volicitin within plants has yet to be reported. Here we present biochemical data that beet armyworm regurgitant serves as a vector for the introduction of volicitin to the site of leaf damage under natural feeding conditions. Corn seedlings were 14CO2-labeled in situ, and beet armyworm larvae were allowed to feed on the labeled leaves. Herbivore oral secretions collected from late-third-instar larvae contained approximately 120 pmol volicitin (0.05 nCi pmol(-1)) per larva. When radiochemically labeled larvae were placed on unlabeled leaves, the amount of volicitin introduced to the damaged site was approximately 5.0 nCi (calc. 100 pmol/larvae). The mobility of volicitin in leaves was examined by allowing radiolabeled beet armyworms to feed on unlabeled plants. In such tracking experiments, radioactivity was not detected in the upper leaves; however, the exogenous application of 5 nCi of [U-14C]sucrose to the lower leaf did result in subsequent radioactivity being detected in the upper portion of the plant. The detection of labeled sucrose with the same radioactivity as that of administered volicitin indicated that volicitin was not readily transported to undamaged leaves and that volicitin may not directly serve as a mobile messenger in triggering the emissions of VOCs systemically.

Antennal multiporous sensilla: their gustatory features for host recognition in female parasitic wasps (insecta, Hymenoptera: Platygastroidea).

In parasitic wasps, various kinds of antennal plates have been interpreted as olfactory organs due to the presence of numerous pores. However, on the basis of ultrastructural investigations, some of these multiporous plates were revealed as being release sites of exocrine glands while others were postulated to have a gustatory function. Such sensilla, present only on female antennae, show unique features, found exclusively in Platygastroidea, with some differences between Scelionidae and Platygastridae. The cuticular apparatus consists of a short basiconic shaft with an apical multiporous area, the pores of which are covered by movable structures. The cellular components are made up of a remarkable number of sensory neurons, from 200 to 220, and an undefined number of sheath cells. These multiporous sensilla have tubular accessory glands that release their secretion through the socket sensillum only in scelionids. These morphological characters, combined with behavioral observations, strongly suggest a gustatory function, although electrophysiological studies are still needed to confirm this. A new terminology for antennal multiporous plates is discussed in relation to their different functions.

Semiochemically mediated foraging behavior in beneficial parasitic insects

AbstractChemical cues enable female parasitic wasps to locate the eggs, larvae, or other life stages of the insects in or on which they place their eggs. These chemical signals, or semiochemicals, may be produced by the hosts and/or by the plants on which the hosts feed. The composition of the chemical signal often differs with different species of hosts or with different plants. New evidence suggests that the wasps exploit semiochemicals emitted by plants in response to insect herbivore feeding. The wasps learn to respond to the different blends of chemicals that indicate the location of their hosts and they can be trained to respond to a specific odor blend. Thus, it may be possible to increase their effectiveness for biological control by conditioning them, prior to their release, to search for a target pest in a particular crop. © 1993 Wiley‐Liss, Inc.

Polydnavirus replication and tissue organization of infected cells in the parasitic wasp Diadegma terebrans

Female parasitic wasps of the species Diadegma terebrans produce a polydnavirus, DtPV, in cells of the calyx. The virus morphology is similar to that of other polydnaviruses. It has a segmented superhelical DNA genome with an estimated size range of 2.3 to 5.5 kilobases. DtPV replication starts within large nuclei where nucleocapsids assemble and become enveloped. They bud through the nuclear envelope and are then "secreted" through the apical microvilli into either the calyx lumen directly or into a channel which is continuous with the lumen. DtPV-producing cells are distributed throughout the length of the calyx and form a discrete, one cell thick "tissue" within it. The large, sector-shaped, DtPV-producing cells form a semicircle around the calyx lumen near the ovariole end of the calyx. This semicircle of DtPV-infected cells increases in circumference towards the lateral oviduct end of the calyx until they completely encircle the lumen and form the major component of the calyx wall.