Transgenerational Plasticity of Maternal Hemolymph Trehalose in Aphids

Aphids exhibit a unique reproductive strategy known as pseudoplacental viviparity, in which embryos develop internally and are thought to receive nutrients such as sugars and amino acids directly from the maternal hemolymph through an ovariole sheath, bypassing the need for traditional yolk storage. This system enables viviparous aphids to adapt to diverse and potentially stressful environments by transmitting maternal environmental cues that influence transgenerational plasticity. However, the mechanisms underlying this nutrient-mediated plasticity are poorly understood. This study focused on the role of trehalose, a primary sugar in the maternal hemolymph, in facilitating adaptive plasticity. Trehalose serves as an energy source and may act as a carrier of environmental information from the mother to offspring, potentially influencing resilience and adaptability. The results showed that winged adult aphids have higher levels of trehalose than wingless morphs, and that these elevated trehalose levels are inherited by their first-instar nymphs. This transfer may help the offspring of winged aphids survive in resource-poor environments after migration. Gene expression analysis showed the upregulation of trehalose metabolism genes in winged adults, possibly to meet the increased energy demands of flight and reproduction. However, trehalose metabolism in embryos appears to be regulated independently of postnatal nutrient uptake. In vitro studies further suggested that trehalose can directly penetrate the oocyte sheath and embryo membrane, supporting a direct pathway for trehalose transfer. These findings highlight the adaptive role of trehalose in aphid development and suggest a potential mechanism for nutrient-based transgenerational plasticity in aphids.