Dual RNA-seq in an aphid parasitoid reveals plastic and evolved adaptation to symbiont-conferred resistance

Coevolving taxa offer the opportunity to study the genetic basis of rapid reciprocal adaptation. We have used experimental evolution to examine adaptation in the parasitoid wasp Lysiphlebus fabarum to resistance conferred by the protective endosymbiont Hamiltonella defensa in its aphid host Aphis fabae. To examine a key stage in parasitoid infection, we have used RNA-seq to study gene expression in 4-5 day old parasitoid larvae contained in still living aphids. With this dual RNA-seq we can simultaneously view expression in individual experimentally evolved parasitoids and the aphids that house them. This gives a view of the sweeping changes in both taxa accompanying successful or unsuccessful infections. Among successful larvae, we find that experimentally evolved populations adapted to H. defensa-protected hosts differ in the expression of genes that include putative toxins and genes to cope with stress. These differences remain even when the larvae are developing in aphids possessing no defensive endosymbionts, suggesting that they are genetically based. In contrast, plastic responses between parasitoids reared in hosts with and without H. defensa are relatively small. Although aphids rely largely on their secondary endosymbionts for defense against parasitoids, we identify expression differences in aphids housing different parasitoid phenotypes. Together, these results demonstrate that wild parasitoid populations possess the genetic variation for rapid adaptation to host resistance, resulting in genetically based differences in gene expression that increase their success in parasitizing symbiont-protected host aphids.