Domestication altered defense responses and host-aphid interaction networks in apples

Abstract

- Domestication can profoundly reshape plant defense strategies and host-parasite interactions, but its consequences for resistance and coevolution in perennial crops remain poorly understood. We investigated how domestication altered apple responses to its major pest, the rosy apple aphid (Dysaphis plantaginea). - We compared wild (Malus orientalis, two geographically differentiated M. sylvestris populations) and cultivated (cider and dessert M. domestica) apple genotypes against two genetically distinct aphid genotypes, combining controlled infestation experiments with phenotypic measurements, paired host-aphid RNA-seq, co-expression network analysis, and genome-wide selection scans. - Aphid fitness and host resistance varied strongly across host populations: domesticated apples supported higher aphid performance, whereas Romanian M. sylvestris showed the highest resistance, revealing marked host-aphid genotype-specific asymmetric compatibility. Cultivated apples have developed extensive inducible transcriptional defense responses, whereas wild populations showed weaker perturbation despite lower aphid fitness, consistent with more constitutive defense. Host-aphid co-expression analyses identified candidate coevolutionary modules linking host resistance genes under balancing selection with aphid genes under positive selection. - Together, these results demonstrate that apple domestication reshaped defense-associated regulatory networks and modified the adaptive landscape experienced by aphid populations, providing new insight into the evolutionary consequences of perennial crop domestication on host-parasite interactions.