Sensory co-evolution: The sex attractant of a gall-making fly primes plant defences, but female flies recognize resulting changes in host-plant quality

Tall goldenrod plants Solidago altissima appear to eavesdrop on the communication of a specialist gall-inducing fly Eurosta solidaginis by detecting the volatile emissions of male flies and priming anti-herbivore defences. However, the effects of defence priming on fly fitness have not previously been demonstrated, despite some evidence that female flies avoid ovipositing on primed plants in the field. To explore how priming affects female preferences and galling success, we manipulated exposure to the priming cue in multiple genotypes of S. altissima and assessed rates of oviposition and gall development. Priming reduced gall formation overall; however, its effect varied across plant genotypes, as well as by the age of the male flies used for priming, possibly reflecting dosage effects (older flies produce lower emissions). Priming by younger males significantly reduced galling success, while priming by older males slightly improved it. Remarkably, female flies accurately assessed host-plant quality by avoiding plants primed by young males while preferring those primed by older males. Synthesis. Our results suggest that defence priming in S. altissima in response to the volatile emissions of E. solidaginis males does affect fly fitness; however, the effect of priming varied by plant genotype, suggesting that there may be variation in defensive strategies against the fly. Female flies have, in response to this defence, evolved a sophisticated ability to evaluate the quality of primed plants.

Automated summary

The tall goldenrod plants have the ability to eavesdrop on communication of gall-inducing flies, priming their defense mechanisms based on male fly emissions. The effects of this defense priming vary depending on plant genotype and male fly age, with younger males reducing galling success and older males slightly improving it. Female flies have evolved the ability to assess plant quality based on these priming cues, avoiding plants primed by younger males and preferring those primed by older males.