Constrained oviposition and female-biased sex allocation in a parasitic wasp

 In haplodiploid organisms such as parasitic wasps, substantial oviposition by females without sperm is predicted to cause mated females to bias their offspring sex ratios towards daughters. The effect of the production of sons by unmated and sperm-depleted (constrained) females on sex allocation by mated females was studied in two populations of the parasitic wasp Bracon hebetor over 3 years. B. hebetor females who depleted their sperm reserves from prior matings rarely remated and became constrained to produce only sons. Constrained females readily oviposited and produced clutches similar in size to those produced by mated females. Although the fraction of constrained females in the population varied considerably between sites and sampling dates, it was usually high enough to favor the production of female-biased sex ratios by mated females. Mated females consistently produced female-biased sex ratios. However, we found no evidence that the sex ratios produced by mated females from the field shifted in relation to the proportion of constrained females in the population. Females held with males or held in isolation also produced female-biased sex ratios. These findings suggest that, in B. hebetor, mated females produce sex ratios that reflect the average fraction of constrained females over evolutionary time. Received: 21 June 1996 / Accepted: 27 August 1996     

Differential dispersal and female-biased sex allocation in a parasitic wasp

1. Differential dispersal of males and females from a population is predicted to result in biased sex-allocation decisions, even in the absence of sibmating.
2. Mated Bracon hebetor Say (Hymenoptera: Braconidae) females produce distinctly female-biased sex ratios (≈ 30% male), yet sibmating is not a feature of the mating biology of this species. Therefore the dispersal behaviour of male and female B. hebetor from caged subpopulations was examined.
3. A higher proportion of females than males dispersed from the caged subpopulations. Furthermore, females dispersed earlier than males. This suggests that the level of competition for mates experienced by males is higher than the level of competition for hosts experienced by sisters.
4. Roughly half of the dispersing females left after they had mated. Females generally mate once in their lifetimes, suggesting that competition between brothers for mates may be high.     

Lipogenesis in an adult parasitic wasp

The goal of this study was to determine the extent of lipogenesis in the parasitoid Eupelmus vuilletti (Hymenoptera: Eupelmidae). Carbohydrate and lipid metabolism were followed in glucose-fed and starved females over 3 days. Fed females increased their glycogen level, while maintaining their lipid level. Starved females used most of their glycogen, while maintaining their lipid level too. Thus, females either use exclusively sugars to preserve their lipid reserves, or maintained a steady renewal of lipids through lipogenesis. The incorporation of radioactively marked glucose into lipids showed however that lipogenesis did not occur at a sufficient level to increase lipid reserves and to compensate for lipid use. This result has important implications for understanding nutrients allocation strategy in this species as the amount of lipids is almost totally fixed upon the emergence. From an evolutionary perspective, we call for detailed physiological studies of lipogenesis in a wide range of adult hymenopterans, as the absence of lipogenesis could be common to all of Aculatea.     

Lifetime gains of host-feeding in a synovigenic parasitic wasp

Abstract. Understanding behavioural decisions relative to host use for feeding or reproduction by foraging parasitoids requires not only the study of metabolic pathways followed by nutrients, but also the quantification of lifetime fitness gains of each alternative behaviour. By using a combination of observational and manipulative approaches, the lifetime host‐feeding gains are measured both in terms of fecundity and longevity in the parasitoid Eupelmus vuilletti. Host‐feeding increases both egg production and longevity. The increase in fecundity is mainly determined by the amount of lipids obtained whereas the lifespan extension is mainly determined by carbohydrates. Proteins obtained through host‐feeding have been implicated previously in egg production by parasitoids but protein intake has no effect on fecundity and longevity in E. vuilletti. The amount of nutrients gained through host‐feeding and invested in eggs is variable and changes over the lifetime of the animal. Therefore, lifetime feeding gains are best understood through the construction of dynamical budgets running over the entire lifespan of an insect.     

Genetic variation in patch time allocation in a parasitic wasp

1. The intra-patch experience acquired by foraging parasitoid females has often been considered to have a strong influence on their tendency to leave a patch, and thus on their total patch residence time. Most studies that have been performed on this subject suggest that the patch-leaving rules observed are adaptive because they enable the females to adjust their patch residence time to local environmental conditions.
2. Considering a behavioural rule as being adaptive supposes that it has been progressively settled by natural selection, and thus that there is, in the population, genetic variation on which the natural selection could act.
3. Therefore, this study aimed to discover whether there was indeed genetic variability in the patch-leaving decision rules in a population of the egg parasitoid species Telenomus busseolae , which attacks patches of its hosts, the eggs of Sesamia nonagrioides . Different wasp families were compared using the isofemale lines method, and the behavioural records were analysed by means of a modified version of the Cox's proportional hazards model proposed by Haccou et al . (1991 ) and Hemerik, Driessen & Haccou (1993 ).
4. The results obtained show that T. busseolae females increase their tendency to leave the patch after each successful oviposition. Each host rejection also led to an increase in the tendency to leave the patch, but this effect was smaller when host rejections were observed between two ovipositions occurring in rapid succession. Subsequent visits to the patch also increased the patch-leaving tendency.
5. Genetic variability was found in both the global patch-leaving tendency and in the effect that successful ovipositions and host rejections have on this tendency.
6. The adaptive and evolutionary consequences of these results are discussed.     

Ambient temperature affects mechanosensory host location in a parasitic wasp

Certain parasitic wasps (Ichneumonidae, Pimplinae) use self-produced vibrations transmitted on plant substrate to locate their immobile concealed hosts (i.e. lepidopteran pupae). This mechanosensory mechanism, called the vibrational sounding, depends both on physical cues of the environment and physical activity of the parasitoid and is postulated to depend on ambient temperature. We analysed the influences of temperature on vibrational sounding by choice experiments using plant-stem models with hidden host mimics in the temperate species Pimpla turionellae. The results show a significant effect of temperature on host-location activity and on the success of this process. Outside an optimum range, the performance of the wasps decreased both at low and high temperatures. Below 10°C and beyond 24°C, the wasps displayed (1) substantial reduction in responsiveness, i.e. proportion of females showing ovipositor insertions, (2) reduction of quantitative activity with ovipositor insertions in the individuals, and (3) reduced precision of mechanosensory host location. Nevertheless, female wasps were able to locate their host over a surprisingly broad range of ambient temperatures which indicates that the wasps are able to compensate for temperature effects on vibrational sounding.     

A learning-related variation in electroantennogram responses of a parasitic wasp

ABSTRACT Odour responses of parasitic insects, in search of their hosts, can change due to experience. Leptopilina heterotoma (Thomson) (Hymenoptera; Eucoilidae), a parasitic wasp of drosophilid larvae, is known to alter its preference for odours emanating from host food substrates through learning. These kinds of behavioural modifications in insects are assumed to be the result of complex processes in the brain. The results presented in this report, however, suggest that this learning-related behavioural variation is not restricted to brain processes but that it involves changes in sensitivity of olfactory receptor neurones.     

Rate of nutrient allocation to egg production in a parasitic wasp

Recent years have seen a marked increase in our awareness of the need to incorporate greater physiological realism into studies of parasitoid behaviour and population dynamics. Quantification of the number of eggs produced as a result of a host-feeding event, the host-feeding gain, is essential for predicting when a parasitoid should bypass an opportunity for current reproduction (i.e. laying eggs) in order to feed from the host and, thus, increase its chances for future reproduction (i.e. producing further eggs). Using radioactively labelled amino acids, one of the main constituents of insect haemolymph, we followed the incorporation of a known quantity of nutrients into each individual egg laid over a long period of time relative to the average life span of the parasitoid. Although the maximum incorporation of nutrients obtained by the female from a discrete feeding event occurs within a short period of time, a large proportion of nutrients are stored and used gradually for egg production throughout the life of the parasitoid. We therefore provide novel experimental evidence showing that feeding gain is not a discrete event in time occurring shortly after feeding, as has so far been assumed, but is instead spread throughout the parasitoid''s lifetime. This has important consequences for calculating the increase in lifetime fitness as a result of a feeding event, a common currency of models that aim to predict feeding and oviposition behaviour in parasitoids.     

Food conversion efficiency of a parasitic wasp, Nemeritis canescens

Abstract. 1. The calorific efficiency with which N. canescens converts the larva of E. kuehniella into its own tissues has been measured by microbomb calorimetry.
2. The calorific values found for Ephestia larvae are high in comparison with those of other insects and may be associated with their high fat content.
3. The growth efficiency of 61% achieved by Nemeritis is sustained by the higher assimilation efficiency of 94%, owing to the parasitoid's habit of feeding directly on the host's haemolymph.
4. The overall efficiency of conversion of adult moth (host) to adult ichneumonid (parasitoid) is of the order of 59% which is broadly representative of endoparasitoids and higher than that achieved by true predators.     

Feeding activity pattern in a parasitic wasp when foraging in the field

Individual decision-making and behavioral plasticity, and hence reproductive success, depend on nutritional state. Despite the importance of food for life-history functions, when and how often parasitoids encounter and consume food in natural settings remain largely unknown. In this study, we aimed at determining the food intake history of the Venturia canescens parasitoids in field conditions. To fulfill this objective, we compared the nutritional state of lab individuals of known feeding history and of field-released individuals allowed to freely forage under natural conditions. Nutritional state and feeding history were determined by using a combination of physiological parameters based on sugar assays. Field-released wasps were caught during periods starting either 5 or 24 h after release. Our results show that in the field, the wasps search actively for carbohydrate food sources. Our work also indicates that feeding activity of wasps in the field can be better understood by using the combination of key physiological parameters. The adaptive value of the feeding pattern and the relevance of the approach used are discussed.     

Species-diagnostic single-nucleotide polymorphism and sequence-tagged site markers for the parasitic wasp genus Nasonia (Hymenoptera: Pteromalidae)

Wasps of the genus Nasonia are important biological control agents of house flies and related filth flies, which are major vectors of human pathogens. Species of Nasonia (Hymenoptera: Pteromalidae) are not easily differentiated from one another by morphological characters, and molecular markers for their reliable identification have been missing so far. Here, we report eight single-nucleotide polymorphism and three sequence-tagged site markers derived from expressed sequenced tag libraries for the two closely related and regionally sympatric species N. giraulti and N. vitripennis. We studied variation of these markers in natural populations of the two species, and we mapped them in the Nasonia genome. The markers are species-diagnostic and evenly spread over all five chromosomes. They are ideal for rapid species identification and hybrid recognition, and they can be used to map economically relevant quantitative trait loci in the Nasonia genome.     

Preimaginal learning determines adult response to chemical stimuli in a parasitic wasp

The behavioural responses of parasitic wasps to chemical cues from their hosts and host plants are known to be affected by genetic and environmental components. In a previous study of the codling moth ectoparasitoid Hyssopus pallidus, we found that the response of adult parasitoids to the frass of their host caterpillars depended on a learning process involving plant cues. In the present study, we investigated how and when learning takes place. A series of experiments was conducted involving exposure of parasitoids to fruit cues at different developmental stages. While parasitoids were not able to learn the fruit cues in the adult stage, exposure to fruit odour at early preimaginal stages significantly increased the adult response to frass from fruit-fed caterpillars. The olfactory memory persisted through metamorphosis, with a retention time of 14 days. Preimaginal learning was not confined to fruit cues but was also demonstrated for a host- and fruit-independent cue, menthol. Parasitoids exposed to menthol odour at the egg and larval stages no longer showed negative responses as adults. Sensitization to fruit cues and habituation to menthol are considered to be the mechanisms involved. This study provides evidence of true preimaginal learning of olfactory cues in a parasitic wasp.     

Characterization of a hymenoptaecin-like antimicrobial peptide in the parasitic wasp Nasonia vitripennis

Hymenoptaecin is a Hymenoptera insect-specific, glycine-rich antimicrobial peptide (AMP) found in non-parasitic bees. Here, we describe a unique hymenoptaecin-like gene (named nahymenoptaecin-1) in the parasitic wasp Nasonia vitripennis, which codes for a larger protein precursor with a carboxyl-terminal hymenoptaecin-like domain (HLD) similar to the bee hymenoptaecin. We recombinantly produced its full-length bioactive form as well as 1–33 and 34–98 fragments (named HLD-n and HLD-c, respectively). Recombinant HLD exhibited activity against Gram-negative and Gram-positive bacteria at micromolar concentrations. Compared to the full-length peptide, HLD-c possessed similar potency in inhibiting the growth of Stenotrophomonus but had a narrower antibacterial spectrum, whereas HLD-n only displayed weak effect on Stenotrophomonus, suggesting that HLD-n is a crucial determinant for bacterial target selectivity while HLD-c represents its active unit for the whole molecule. Circular dichroism analysis combined with ab initio structure prediction by Robetta indicated that HLD-n adopts a random coil conformation whereas glycine-rich HLD-c forms a loose β-sheet structure. Relative to bee hymenoptaecin, the upstream region of HLD contains two accurately repeated proline-rich AMP-like peptides instead of an acidic propeptide. Such difference could be a consequence of exon shuffling of autonomous modules after speciation.     

Inheritance of gynandromorphism in the parasitic wasp Nasonia vitripennis

The parasitic wasp Nasonia vitripennis has haplo-diploid sex determination. Males develop from unfertilized eggs and are haploid, whereas females develop from fertilized eggs and are diploid. Females and males can be easily distinguished by their morphology. A strain that produces individuals with both male and female features (gynandromorphs) is studied. We provide data on female/male patterning within and between individuals, on environmental effects influencing the occurrence of gynandromorphism, and on its pattern of inheritance. A clear anterior/posterior pattern of feminization is evident in gynandromorphic individuals that developed from unfertilized haploid eggs. The proportion of gynandromorphic individuals can be increased by exposing the mothers to high temperature and also by exposing embryos at early stages of development. Selection for increased gynandromorph frequency was successful. Backcross and introgression experiments showed that a combination of a nuclear and a heritable cytoplasmic component causes gynandromorphism. Analyses of reciprocal F(2) and F(3) progeny indicate a maternal effect locus (gyn1) that maps to chromosome IV. Coupled with previous studies, our results are consistent with a N. vitripennis sex determination involving a maternal/zygotic balance system and/or maternal imprinting. Genetics and temperature effects suggest a temperature-sensitive mutation of a maternally produced masculinizing product that acts during a critical period in early embryogenesis.     

Flight manoeuvers used by a parasitic wasp to locate host-infested plant

Cotesia rubecula Marshall (Hymenoptera: Braconidae) is a specialist larval parasitoid of the butterfly Pieris rapae L. which itself feeds almost exclusively upon cruciferous plants. Female wasps are attracted to the odour of host-infested plant (plant-host complex: PHC) and the probability of flights in a wind tunnel depends on females' prior oviposition experience with the PHC and on the concentration of the PHC odour. This study considers the effect of both factors on characteristics of oriented flight upwind towards the PHC. The flight track parameters that we measured and calculated were not significantly affected by these factors. C. rubecula females exhibited high average flight velocity and relatively straight flight tracks. There was a considerable variability between individuals, however, in their odour-modulated upwind flight tracks. Some females generated a zigzagging upwind flight track similar to those commonly observed from male moths responding to female sex pheromone. Other females flew along a straight track directly upwind. The flight tracks of most female wasps were intermediate between these extremes. The full range of these flight performances was observed to all experimental treatments.