Alex R. Kraaijeveld

Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster.

The extent to which an organism is selected to invest in defences against pathogens and parasites depends on the advantages that ensue should infection occur, but also on the costs of maintaining defences in the absence of infection. The presence of heritable variation in resistance suggests that costs exist, but we know very little about the nature or magnitude of these costs in natural populations of animals. A powerful technique for identifying trade-offs between fitness components is the study of correlated responses to artificial selection. We have selected Drosophila melanogaster for improved resistance against an endoparasitoid, Asobara tabida. Endoparasitoids are insects whose larvae develop internally within the body of other insects, eventually killing them, although their hosts can sometimes survive attack by mounting a cellular immune response. We found that reduced larval competitive ability in unparasitized D. melanogaster is a correlated response to artificial selection for improved resistance against A. tabida. The strength of selection for competitive ability and parasitoid resistance is likely to vary temporally and spatially, which may explain the observed heritable variation in resistance.

Basis of the trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster.

Drosophila melanogaster can be artificially selected for increased resistance against parasitoid wasps that attack the larvae. Lines selected for greater resistance are poorer larval competitors under conditions of resource scarcity. Here we investigated the mechanistic basis of this apparent trade–off. We found that resistant lines have approximately twice the density of haemocytes (blood cells) than that of controls. Haemocytes are involved in encapsulation, the chief cellular immune defence against parasitoids. We have previously shown that resistant lines feed more slowly than controls and hypothesize that limiting resources are being switched from trophic to defensive functions.

Trade–off associated with selection for increased ability to resist parasitoid attack in Drosophila melanogaster

Costs of resistance are widely assumed to be important in the evolution of parasite and pathogen defence in animals, but they have been demonstrated experimentally on very few occasions. Endoparasitoids are insects whose larvae develop inside the bodies of other insects where they defend themselves from attack by their hosts’ immune systems (especially cellular encapsulation). Working with Drosophila melanogaster and its endoparasitoid Leptopilina boulardi, we selected for increased resistance in four replicate populations of flies. The percentage of flies surviving attack increased from about 0.5% to between 40% and 50% in five generations, revealing substantial additive genetic variation in resistance in the field population from which our culture was established. In comparison with four control lines, flies from selected lines suffered from lower larval survival under conditions of moderate to severe intraspecific competition.

CLONAL VARIATION AND COVARIATION IN APHID RESISTANCE TO PARASITOIDS AND A PATHOGEN

Abstract The potential rate of evolution of resistance to natural enemies depends on the genetic variation present in the population and any trade-offs between resistance and other components of fitness. We measured clonal variation and covariation in pea aphids (Acyrthosiphon pisum) for resistance to two parasitoid species (Aphidius ervi and A. eadyi) and a fungal pathogen (Erynia neoaphidis). We found significant clonal variation in resistance to all three natural enemies. We tested the hypothesis that there might be trade-offs (negative covariation) in defensive ability against different natural enemies, but found no evidence for this. All correlations in defensive ability were positive, that between the two parasitoid species significantly so. Defensive ability was not correlated with fecundity. A number of aphid clones were completely resistant to one parasitoid (A. eadyi), but a subset of these failed to reproduce subsequently. We discuss the factors that might maintain clonal variation in natural enemy resistance. Corresponding Editor: T. Kawecki

Genome-wide gene expression in response to parasitoid attack in Drosophila

BackgroundParasitoids are insect parasites whose larvae develop in the bodies of other insects. The main immune defense against parasitoids is encapsulation of the foreign body by blood cells, which subsequently often melanize. The capsule sequesters and kills the parasite. The molecular processes involved are still poorly understood, especially compared with insect humoral immunity.ResultsWe explored the transcriptional response to parasitoid attack in Drosophila larvae at nine time points following parasitism, hybridizing five biologic replicates per time point to whole-genome microarrays for both parasitized and control larvae. We found significantly different expression profiles for 159 probe sets (representing genes), and we classified them into 16 clusters based on patterns of co-expression. A series of functional annotations were nonrandomly associated with different clusters, including several involving immunity and related functions. We also identified nonrandom associations of transcription factor binding sites for three main regulators of innate immune responses (GATA/srp-like, NF-κB/Rel-like and Stat), as well as a novel putative binding site for an unknown transcription factor. The appearance or absence of candidate genes previously associated with insect immunity in our differentially expressed gene set was surveyed.ConclusionMost genes that exhibited altered expression following parasitoid attack differed from those induced during antimicrobial immune responses, and had not previously been associated with defense. Applying bioinformatic techniques contributed toward a description of the encapsulation response as an integrated system, identifying putative regulators of co-expressed and functionally related genes. Genome-wide studies such as ours are a powerful first approach to investigating novel genes involved in invertebrate immunity.

The coevolution of host resistance and parasitoid virulence

Host-parasitoid interactions are abundant in nature and offer great scope for the study of coevolution. A particularly fertile area is the interaction between internal feeding parasitoids and their hosts. Hosts have evolved a variety of means of combating parasitoids, in particular cellular encapsulation, while parasitoids have evolved a wide range of countermeasures. Studies of the evolution of host resistance and parasitoid virulence are reviewed, with an emphasis on work involving Drosophila and its parasitoids. Genetic variation in both traits has been demonstrated using isofemale line and artificial selection techniques. Recent studies have investigated the fitness costs of maintaining the ability to resist parasitoids, the comparative fitness of flies that have successfully defended themselves against parasitoids, and the degree to which resistance and virulence act against one or more species of host or parasitoid. A number of studies have examined geographical patterns, and sought to look for local adaptation; or have compared the traits across a range of species. Finally, the physiological and genetic basis of change in resistance and virulence is being investigated. While concentrating on Drosophila, the limited amount of work on different systems is reviewed, and other possible areas of coevolution in host-parasitoid interactions are briefly discussed.

Cross-resistance following artificial selection for increased defense against parasitoids in Drosophila melanogaster

An increase in resistance to one natural enemy may result in no correlated change, a positive correlated change, or a negative correlated change in the ability of the host or prey to resist other natural enemies. The type of specificity is important in understanding the evolutionary response to natural enemies and was studied here in a Drosophila‐paxasitoid system. Drosophila melanogaster lines selected for increased larval resistance to the endoparasitoid wasps Asobara tabida or Leptopilina boulardi were exposed to attack by A. tabida, L. boulardi and Leptopilina heterotoma at 15°C, 20°C, and 25°C. In general, encapsulation ability increased with temperature, with the exception of the lines selected against L. boulardi, which showed the opposite trend. Lines selected against L. boulardi showed large increases in resistance against all three parasitoid species, and showed similar levels of defense against A. tabida to the lines selected against that parasitoid. In contrast, lines selected against A. tabida showed a large increase in resistance to A. tabida and generally to L. heterotoma, but displayed only a small change in their ability to survive attack by L. boulardi. Such asymmetries in correlated responses to selection for increased resistance to natural enemies may influence host‐parasitoid community structure.

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.

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.

Association between feeding rate and parasitoid resistance in Drosophila melanogaster

Replicate lines of Drosophila melanogaster have been selected for increased resistance against one of two species of parasitoid wasp, Asobara tabida and Leptopilina boulardi. In both cases, it has been shown that an improved ability to mount an immunological defense against the parasitoids egg is associated with reduced survival when the larvae are reared under conditions of low resource availability and thus high competition. We show here that in both sets of selected lines, lower competitive ability is associated with reduced rates of larval feeding, as measured by the frequency of retractions of the cephalopharyngeal skeleton. This suggests that the same or similar physiological processes are involved in the trade‐off between competition and resistance against either parasitoid and shows how the interaction between adaptations for competition and natural enemy resistance may be mediated.