Lack of phenotypic and evolutionary cross-resistance against parasitoids and pathogens in Drosophila melanogaster

Abstract

Background: When organisms are attacked by multiple natural enemies, the evolution of a resistance mechanism to one natural enemy will be influenced by the degree of cross-resistance to another natural enemy. Cross-resistance can be positive, when a resistance mechanism against one natural enemy also offers resistance to another; or negative, in the form of a trade-off, when an increase in resistance against one natural enemy results in a decrease in resistance against another. Using Drosophila melanogaster, an important model system for the evolution of invertebrate immunity, we test for the existence of cross-resistance against parasites and pathogens, at both a phenotypic and evolutionary level.

Methods: We used a field strain of D. melanogaster to test whether surviving parasitism by the parasitoid Asobara tabida has an effect on the resistance against Beauveria bassiana, an entomopathogenic fungus; and whether infection with the microsporidian Tubulinosema kingi has an effect on the resistance against A. tabida. We used lines selected for increased resistance to A. tabida to test whether increased parasitoid resistance has an effect on resistance against B. bassiana and T. kingi. We used lines selected for increased tolerance against B. bassiana to test whether increased fungal resistance has an effect on resistance against A. tabida.

Results/conclusions: We found no positive cross-resistance or trade-offs in the resistance to parasites and pathogens. This is an important finding, given the use of D. melanogaster as a model system for the evolution of invertebrate immunity. The lack of any cross-resistance to parasites and pathogens, at both the phenotypic and the evolutionary level, suggests that evolution of resistance against one class of natural enemies is largely independent of evolution of resistance against the other.

Figure 1. Fungal resistance of flies surviving parasitism.

Mean time to death (in days) for Drosophila melanogaster adult flies that were either infected with Beauveria bassiana (F; grey bars) or uninfected (U; white bars), depending on whether they had been parasitised by Asobara tabida as a larvae (Par; right side of panel) or had not been parasitised (Unp; left side of panel). The two bars within each treatment combination represent the results of the two experimental blocks. Bars show mean ± s.e.

Figure 2. Encapsulation ability of larvae infected with microsporidia.

Rate of encapsulation of Asobara tabida eggs by Drosophila melanogaster larvae which had either been infected with Tubulinosema kingi (M; grey bar) or had not been infected (U; white bar). Bars show mean ± s.e.

Figure 3. Fungal resistance of flies selected for parasitoid resistance.

Mean time to death (in days) for Drosophila melanogaster adult flies that were either infected with Beauveria bassiana (F; grey bars) or uninfected (U; white bars), depending on whether they had been selected for increased resistance to Asobara tabida (Sel; right side of panel) or had not been selected (Con; left side of panel). Bars show mean ± s.e.

Figure 4. Resistance to microsporidia of flies selected for parasitoid resistance.

Early fecundity of Drosophila melanogaster females adult flies that were either infected with Tubulinosema kingi (M; grey bars) or uninfected (U; white bars), depending on whether they had been selected for increased resistance to Asobara tabida (Sel; right side of panel) or had not been selected (Con; left side of panel). Bars show mean ± s.e.

Figure 5. Encapsulation ability of larvae selected for fungal resistance.

Rate of encapsulation of Asobara tabida eggs by Drosophila melanogaster larvae which had either been selected for tolerance to Beauveria bassiana (S; grey bar) or had not been selected (U; white bar). Bars show mean ± s.e.