Experimental evolution of defense against a competitive mold confers reduced sensitivity to fungal toxins but no increased resistance in Drosophilalarvae

Abstract

BackgroundFungal secondary metabolites have been suggested to function as chemical defenses against insect antagonists, i.e. predators and competitors. Because insects and fungi often compete for dead organic material, insects may achieve protection against fungi by reducing sensitivity to fungal chemicals. This, in turn, may lead to increased resistance allowing insects better to suppress the spread of antagonistic but non-pathogenic microbes in their habitat. However, it remains controversial whether fungal toxins serve as a chemical shield that selects for insects that are less sensitive to toxins, and hence favors the evolution of insect resistance against microbial competitors.ResultsTo examine the relationship between the ability to survive competition with toxic fungi, sensitivity to fungal toxins and resistance, we created fungal-selected (FS) replicated insect lines by exposing Drosophila melanogaster larvae to the fungal competitor Aspergillus nidulans over 26 insect generations. Compared to unselected control lines (UC), larvae from the FS lines had higher survival rates in the presence of A. nidulans indicating selection for increased protection against the fungal antagonist. In line with our expectation, FS lines were less susceptible to the A. nidulans mycotoxin Sterigmatocystin. Of particular interest is that evolved protection against A. nidulans and Sterigmatocytin was not correlated with increased insect survival in the presence of other fungi and mycotoxins. We found no evidence that FS lines were better at suppressing the expansion of fungal colonies but observed a trend towards a less detrimental effect of FS larvae on fungal growth.ConclusionAntagonistic but non-pathogenic fungi favor insect variants better protected against the fungal chemical arsenal. This highlights the often proposed but experimentally underexplored importance of secondary metabolites in driving animal-fungus interactions. Instead of enhanced resistance, insect larvae tend to have evolved increased tolerance of the fungal competitor. Future studies should examine whether sensitivity to allelopathic microbial metabolites drives a trade-off between resistance and tolerance in insect external defense.

Can Insects Develop Resistance to Insect Pathogenic Fungi?

“…In the absence of fungal infection, these selected flies had lower fitness than control flies indicating a trade off with increased tolerance [30]. In another study, exposure of D. melanogaster over twenty six generations to an antagonistic (but not true insect-pathogenic) fungus Aspergillus nidulans , resulted in selected lines with no increase in resistance but a reduced sensitivity to sterigmatocystin, a toxin produced by this fungus [31]. The underlying mechanism(s) for the increased toxin specific tolerance is unclear.…”

Induced Fungal Resistance to Insect Grazing: Reciprocal Fitness Consequences and Fungal Gene Expression in the Drosophila-Aspergillus Model System

“…Overexpression of rsmA has recently been shown to result in enhanced sterigmatocystin biosynthesis coupled with strong feeding avoidance by fungivorous collembolans [33], and sterigmatocystin strongly affects D. melanogaster development [34]. Despite the apparent activation of regulatory elements of the sterigmatocystin cluster it is interesting that stcA which encodes an early biosynthetic enzyme of the sterigmatocystin pathway was not differentially expressed.…”

Bayesian updating during development predicts genotypic differences in plasticity

“…In nature, the presence of aversive stimuli in a microhabitat that emits a given odor (in this case, ethyl acetate) is relevant to D. melanogaster larvae because microhabitat quality not only depends on food quantity and quality, but also on other factors, including the moisture and texture of the substrate (Del Pino et al. ; Johnson and Carder ), the presence of toxin‐producing fungi (Trienens and Rohlfs ), and the chances of encountering parasites or parasitoids (Fleury et al. ; Hamilton et al.…”