A Novel Gene REPTOR2 Activates the Autophagic Degradation of Wing Disc in Pea Aphid

Wing dimorphism is an evolutionarily adaptive trait to maximize insect fitness under various environments, by which the population could be balanced between migration and reproduction. Most studies concern the regulatory mechanisms underlying the stimulation of wing morph in aphids, but relatively little research addresses the molecular basis of wing loss. Here, we found that the wing disc of wingless-destined pea aphids degenerated 30 h post birth by autophagic rather than apoptotic degeneration, whereas winged-destined aphids developed normally. Activation of autophagy in 1^st instar nymphs reduced the proportion of winged aphids, and suppression of autophagy increased the proportion. The REPTOR2 gene associated with TOR signaling pathway was identified by RNA-seq as a differentially expressed gene between the two morphs, with higher expression in the thorax of wingless-destined aphids. Further genetic analysis indicated that REPTOR2 could be a novel gene derived from a gene duplication event exclusively in pea aphid on autosome A1 but translocated to the sex chromosome. Knockdown of REPTOR2 reduced autophagy in the wing disc and increased the proportion of winged aphids. In agreement with REPTOR’s canonical negative regulatory role of TOR on autophagy, winged-destined aphids had higher TOR expression in the wing disc. Suppression of TOR activated autophagy of the wing disc and decreased the proportion of winged aphids, and vice versa. These results revealed that the TOR signaling pathway controlled degradation of the wing disc in pea aphids, and that REPTOR2 could modulate this autophagic degradation.