In Europe, the most common parasitoid species attacking larvae of D. melanogaster (and related species) are the braconid Asobara tabida and the figitids Leptopilina boulardi and Leptopilina heter-otoma (Carton et al., 1986). In addition, the most common species attacking Drosophila pupae is Pachycrepoideus vindemmiae (Carton et al., 1986). As, by definition, parasitoids kill their host as part of their normal development, the fitness loss for a Drosophila not defending itself against parasit-oid attack and encapsulating the parasitoid egg is very high: death in the pupal stage; that is, before becoming reproductively active. Rates of parasitism by parasitoids can reach very high levels (up to 70%) in field populations of Drosophila (Carton et al., 1991; Fleury et al., 2004). Despite parasitoids being so common, and the fitness consequences of parasitoid attack being potentially severe, field populations of D. melanogaster show a considerable amount of variation in resistance against parasitoids, both between and within populations (Carton and Bouletreau, 1985; Kraaijeveld and van Alphen, 1995).
As explained above, costs of resistance, coupled with temporal and/or spatial variation in rates of parasitism, could explain the maintenance of this genetic variation in resistance. In D. melanogaster, surviving parasitoid attack has been shown to bear costs. Parasitized larvae have a lower competitive ability (Tien et al., 2001) than unparasitized larvae. After pupation, larvae which have successfully encapsulated the parasitoid egg have an increased risk of being attacked by pupal parasitoids (Fellowes et al., 1998b). Adult flies which succeeded in encapsulating the parasitoid egg as larvae are smaller than flies which were not parasitized, with females having lower fecundity and males having lower mating success (Carton and David, 1983; Fellowes et al., 1999a). Presumably, these costs are a result of the larva redirecting resources to its immune response, although pathogenic effects cannot be ruled out.
Investment in an immune system, in anticipation of being parasitized, is also costly in D. mel-anogaster. Using replicated artificial selection, Kraaijeveld and Godfray (1997) and Fellowes et al. (1998a) showed that high resistance against both A. tabida and L. boulardi can be selected for. Larvae from lines selected for increased parasitoid resistance, have higher levels of circulating haemo-cytes (Kraaijeveld et al., 2001). However, this high resistance is correlated with a reduced feeding rate and a reduction in competitive ability (Kraaijeveld and Godfray, 1997; Fellowes et al, 1998a, 1999b). Interestingly, replicated selection for increased competitive ability leads to an increase in parasit-oid resistance (Sanders et al., 2005), possibly as a result of selection for increased wound-healing ability under crowded conditions. This shows that the trade-off between resistance and competitive ability is potentially asymmetrical. The trade-off appears more complex than one involving just haemocyte numbers and feeding rate, and traits other than these two may be involved.
As the pupal parasitoids attacking Drosophila are ectoparasitoids, their eggs do not come into contact with the host's immune system. The only barrier that parasitoids need to breach, the puparial wall, does not appear to be able to act as a 'resistance mechanism', as variation in the thickness of the puparial wall is not correlated to variation in risk of parasitism (Kraaijeveld and Godfray, 2003). Therefore, the only 'defence' that Drosophila pupae have against pupal parasitoids is to reduce the probability of being parasitized in the first place. The size of a pupa plays a role in its probability of being found and attacked by a searching para-sitoid female (Kraaijeveld and Godfray, 2003), so a population under attack from pupal parasitoids is expected to evolve towards a smaller pupal size. Pupal and adult sizes are strongly correlated, so the cost of avoiding attack by pupal parasitoids is a reduction in adult size (Kraaijeveld and Godfray, 2003), leading to a decrease in a range of fitness parameters such as mating success, fecundity, and dispersal.
Drosophila nigrospiracula, which feeds on rotting cactus tissue, is susceptible to parasitism by the facultative ectoparasitic mite Macrocheles subbadius. The mites use flies as a means of dispersal, but also consume host haemolymph (Polak and Markow, 1995; Polak, 1996, 2003; Luong and Polak, 2007a, 2007b). The prevalence of mites in field populations is variable, but can reach levels of over 30% of flies infected (Polak and Markow, 1995). Infected flies suffer a reduction in longevity, fecundity, and mating success, with the size of the reduction depending on the number of mites attached (Polak and Markow, 1995; Polak, 1996).
Resistance of flies against the mites is not immunological, but behavioural: sudden movements are used to prevent mites getting a hold and tarsal flicking dislodges mites that have taken a hold (Polak, 2003). Genetic variation for this behavioural resistance exists in natural populations (Polak, 2003), which, as in the case of parasitoid resistance discussed above, suggests that behavioural resistance bears a cost.
The energetic costs of the movements and flicks are unknown, but selection for increased behavioural resistance leads to a decrease in larval competitive ability, adult body size, and fecundity (Luong and Polak, 2007a, 2007b), suggesting that the resistance mechanism is indeed costly.
Several species of nematodes are obligate parasites of Drosophila. Species of the quinaria and testacea groups feeding on decaying mushrooms are primarily attacked by nematodes in the genus Howardula, whereas species of the obscura group feeding on fermenting fruits are attacked by Parasitylenchus diplogenus (Welch, 1959; Montague and Jaenike, 1985; Jaenike, 1992). Parasitism starts with a single free-living worm entering a Drosophila larva, which is then followed by the production of one or two generations in the fly as it reaches adulthood. The worms then leave the fly abdomen in search of new host larvae to parasitize (Welch, 1959). In the case of Parasitylenchus, the abdomen of an infected fly can contain thousands of worms (A.R. Kraaijeveld, personal observation).
The abundance of nematodes in field populations can be as high as 35% of individuals of quinaria group species parasitized by Howardula (Montague and Jaenike, 1985). In the case of Parasitylenchus, rates of parasitism in flies of obscura group species have been reported as 3% (Gillis and Hardy, 1997), but can go up to 10% (A.R. Kraaijeveld, unpublished results). D. melanogaster is susceptible to infection by Parasitylenchus in the laboratory (Welch, 1959), but there are no records of infection of D. mela-nogaster by nematodes in field populations.
Infected flies suffer from increased mortality and, in the case of females, from being effectively sterilized. This female sterilization occurs after infection with Howardula (Jaenike, 1992; Jaenike et al., 1995) and Parasitylenchus (A.R. Kraaijeveld, unpublished results).
Resistance of Drosophila against parasitism by nematodes has not been recorded, although encapsulation is recorded in other Diptera (Stoffolano, 1973). As such, nothing is known about any resistance mechanism against nematodes that Drosophila may employ, or about the costs of resistance to nematodes.
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