Stephen F. Hubbard

Wolbachia infection suppresses both host defence and parasitoid counter-defence

Endosymbiotic bacteria in the genus Wolbachia have been linked to several types of reproductive parasitism, which enhance their own transmission, while their direct effects on the host vary from beneficial to neutral or detrimental. Here, we report negative effects of infection on immunity-related traits of Drosophila simulans and the parasitoid wasp Leptopilina heterotoma. Infected D. simulans showed a reduced ability to encapsulate parasitoid eggs, compared to a tetracycline-treated, bacterium-free line. Challenging the two lines with a fungal pathogen, Beauveria bassiana, on the other hand, revealed no differences in survival. Moreover, elimination of Wolbachia was beneficial for the parasitoid wasp, as eggs laid by uninfected females suffered significantly lower encapsulation rates. We discuss possible origins of these fitness costs and their implications for infection dynamics and the interactions between host species.

The perception of genetic similarity by the solitary parthenogenetic parasitoid Venturia canescens, and its effects on the occurrence of superparasitism

Observations of oviposition patterns adopted by uniparental lines of the solitary parthenogenetic endoparasitoid Venturia canescens Gravenhorst (Hymenoptera: Ichneumonidae) reveal that the occurrence of superparasitism is influenced by the genealogical relationship between adult wasps and conspecific progeny which they encounter within parasitized hosts (larvae of the Indian meal moth Plodia interpunctella Hübner (Lepidoptera: Pyralidae)): the closer the relationship, the lower the occurrence of superparasitism. This behaviour has an adaptive interpretation because it allows Venturia to avoid selective penalties incurred when larval offspring compete with genetically similar progeny. Venturias ability to discriminate between her own eggs, those of her relatives, and those of other conspecifics is mediated by a chemical marker produced by Dufours gland, an accessory of the adult females reproductive system. This conclusion is supported by chemical analyses which reveal that, while Dufours glands from unrelated females show highly significant variation between the spectra of volatile hydrocarbons contained in their respective secretions, closely‐related females show negligible differences in their chemical constitutions. These findings lend further weight to current theory that superparasitism can be deliberately deployed as an adaptive part of a wasps behavioural repertoire, and also identify the physiological mechanism by which such an oviposition response may be achieved.

Host-searching behavior ofVenturia canescens (Grav.) (Hymenoptera: Ichneumonidae): Interference—the effect of mature egg load and prior behavior

The foraging behavior ofVenturia canescens, a solitary endoparasitoid of lepidopteran larvae, was investigated in the laboratory. Females with a greater number of mature eggs in their ovarioles and oviducts parasitized a greater number of hosts and won a greater proportion of encounters with other searching females. Wasps which had been exposed to hosts prior to an experimental trial lost a higher proportion ofagonistic encounters with conspecifics than wasps which had no prior exposure to hosts. The behavior of a wasp at the time of the encounter influenced the outcome of the encounter. Wasps involved in active search of the host medium with the ovipositor (“probing”) were more likely to win encounters than wasps in any other behavioral category. In a situation where the agonistic encounter was between two probing wasps, both contestants were equally likely to win. Results are discussed in the light of the idea that mutual interference arises, in this species, as a result of agonistic encounters between searching females and recent dynamic-programming models which suggest that parasitoid oviposition should be influenced by mature egg load.

The essential properties of evolutionary stability

We show that the “standard conditions” for evolutionarily stable strategies proposed by Maynard Smith & Price (1973) are sometimes inconsistent with the notion of dynamic stability. We suggest, therefore, that the criteria of dynamic stability should be used in place of the standard conditions in assessing stability in phenotypic models of evolution. Strategy mixtures satisfying the condition of dynamic stability are termed evolutionarily stable points. An algorithm is presented which will locate all evolutionarily stable points for any discrete, linear contest.

Avoidance of superparasitism : a matter of learning ?

Superparasitism (laying eggs into parasitized hosts) by solitary parasitoids was regarded for a long time as a mistake on the part of the foraging parasitoid, but is now widely accepted as often adaptive. In Venturia canescens the rate of avoidance of superparasitism has been shown to rise over the first 20 min from the deposition of the first egg, possibly because of a constraint in the detectability of the marker used to label parasitized hosts. Here, we show that the increase in avoidance of superparasitism with time is the result of a females experience of hosts in the interval between laying an egg in a host and re-encountering that same host. Wasps deprived of hosts in this interval showed no avoidance of superparasitism; those given healthy hosts every 3 min during this interval showed increasing avoidance of superparasitism with time. Furthermore, the marker was detectable in a host within 3 min of oviposition. The results suggest that wasps quickly acquire information about the abundance of healthy hosts in their environment, and base their decision to superparasitize on this information. Copyright 1999 The Association for the Study of Animal Behaviour.

Combining plant resistance and a natural enemy to control Amphorophora idaei

The European large raspberry aphid Amphorophora idaei Börner (Homoptera: Aphididae) is a virus vector of at least four plant virus complexes making it the most important aphid pest of raspberries in Northern Europe. An approach combining a bottom-up control (plant resistance) and a top-down control (an aphid parasitoid) using Aphidius ervi Haliday (Hymenoptera: Aphidiinae) was investigated in the laboratory. Aphid performance (pre-reproductive period, total reproductive output, lifespan and rm) were compared when reared on both a susceptible cultivar and a resistant cultivar with significantly poorer performance on the resistant cultivar. Parasitoid attack behaviour increased with aphid density on both cultivars, but was significantly lower on resistant plants than susceptible plants. Aphids showed a greater tendency to drop from the plant when feeding on resistant plants compared with susceptible plants. The significance of the results is discussed in the context of possible control of the aphid using these combined methods.

Microsatellite frequency and size variation in the parthenogenetic parasitic wasp Venturia canescens (Gravenhorst) (Hymenoptera: Ichneumonidae)

Nine genomic libraries of the parthenogenetic wasp Venturia canescens were screened for microsatellite loci. In contrast to other Hymenoptera (GT)n and not (CT)n, was the predominant repeat category found with 14 kb and 28 kb genomic DNA between loci, respectively. Mono‐ and trinucleotide microsatellites were rarer, occurring at frequencies between 231 kb and 589 kb of genome, whilst tetranucleotide repeats are scarce, with (ATTC)n and (CCGG)n loci occurring every 692 kb and 983 kb, respectively, and only one small imperfect (GATA)n locus and no (GACA)n loci were revealed. Over 70% of the dinucleotide, and all the trinucleotide microsatellites were small (less than eleven repeats), whilst 60% to 80% of loci were imperfect. Moreover, very few compound microsatellites and only a single association between different microsatellites were observed.

Protection of Pea Aphids Associated with Coinfecting Bacterial Symbionts Persists During Superparasitism by a Braconid Wasp

Bacterial endosymbionts that associate facultatively with insect herbivores can influence insect fitness and trophic interactions. The pea aphid, Acyrthosiphon pisum, can be protected from parasitism by the braconid wasp Aphidius ervi when harbouring particular symbiotic bacteria, with specific endosymbiont coinfections providing almost complete protection. However, studies often quantify aphid mummification with no control over parasitoid oviposition per aphid; thus, if mummy production fails or is low, the causes are often unclear. Here, we show that the high level of protection associated with the coinfecting endosymbionts Hamiltonella defensa and X-type is maintained even when pea aphids are superparasitised. This contrasts strongly with the protection provided by H. defensa alone, which has been shown by others to be overcome by superparasitism. By dissecting aphids exposed to two parasitoid attacks, we reveal that A. ervi deposits eggs equally freely in endosymbiont-infected and uninfected nymphs, and lack of mummification in endosymbiont-protected nymphs arises from failure of the wasp eggs to hatch or emerging larvae to develop.

Disease induced dynamics in host–parasitoid systems: chaos and coexistence

All animals and plants are, to some extent, susceptible to disease caused by varying combinations of parasites, viruses and bacteria. In this paper, we present a mathematical model of interactions between a host, two parasitoids and a pathogen which shows that the presence of an infection can preserve and promote diversity in such multi-species systems. Initially, we use a system of ordinary differential equations to investigate interactions between two species of parasitoids, a host and a host infection. We show that the presence of all four species is necessary for the system as a whole to persist, and that in particular, the presence of the pathogen is necessary for the coexistence of the two parasitoid species. The inclusion of infection induces a wide range of dynamics, including chaos, and these dynamics are robust for a wide range of parameter values. We then extend the model to include spatial effects by introducing random motility (diffusion) of all three species and examine the subsequent spatio-temporal dynamics, including travelling waves and other more complicated heterogeneous behaviour. The computational simulation results of the model suggest that infection in the hosts can blunt the effects of competition between parasitoids, allowing the weaker competitor to survive. Regardless of the nature of the stability of the coexistent steady state of the system, there is an initial period of transient dynamics, the length of which can be extended by an appropriate choice of initial conditions. The existence of these transient dynamics suggests that systems subject to regular restoration to a starting state, such as agro-ecosystems, may be kept in a continual state of dynamic transience, and this has implications for the use of natural enemies to control insect pests, the preservation of biodiversity in farmland habitats and the more general dynamics of disease processes.

Host-searching behavior of Venturia canescens (Grav.) (Hymenoptera : Ichneumonidae) : Superparasitism

The foraging behavior ofVenturia canescens, a solitary endoparasitoid of lepidopteran larvae, was investigated in the laboratory. FemaleVenturia canescens with a larger number of mature eggs to lay were found to have higher levels of superparasitism (measured as numbers of eggs laid per parasitized host). Increased parasitoid density was found to result in reduced levels of superparasitism by host-deprived (i.e.,undepleted) wasps. Females which had been allowed access to hosts before the experiment (depleted wasps) laid fewer eggs per parasitized host than undepleted wasps, although there was no significant difference in the levels of superparasitism among the depletion periods of 1, 2, 5, and 7 h. It was also found that an egg which was encountered less than 15 min after oviposition was much less likely to be avoided than one which was encountered after more than 15 min had elapsed.