Optimal sugar components provide essential cues for the formation of host‐specialised cotton‐melon aphids

Abstract Host specialisation is a common phenotype in herbivores and is considered as an important driver for species diversity of herbivores. Previous studies have revealed that a distinct plant defence mechanism underlies herbivores' host specialisation. However, the role of plant nutritional status, especially sugar metabolism, is a widely overlooked driver of host specialisation formation. Here, the Cucurbitaceae biotype (CA) and Malvaceae biotype (MA) of cotton‐melon aphids, Aphis gossypii , were used to reveal the potential role of plant sugar metabolism in the formation of host‐specialised aphid biotypes. The abundance, intrinsic rate of increase and net reproductive rate of CA and MA biotypes significantly decreased after reciprocal host transfer, suggesting a host utilisation trade‐off between these biotypes. Further analysis of sugar quality showed differences in sugar components, especially raffinose‐family oligosaccharides (RFOs), between watermelon and cotton plants. The concentrations and ratios of raffinose and stachyose were higher in watermelon leaves than in cotton leaves, respectively. Exogenous application of different sugar substrates showed that CA biotypes performed the best on artificial diets with sucrose and raffinose (3:8) while MA biotypes established populations on artificial diets with only sucrose. Moreover, the level of aphid's galactosidase activity, a key enzyme in RFOs metabolism, decreased in CA biotypes but increased in MA biotypes after reciprocal host transfer for acclimatising themselves to changes in RFOs of host plants. Consequently, optimal sugar components provide essential cues for the formation of host‐specialised cotton‐melon aphids.