Drosophila larval epidermal cells only exhibit epidermal aging when they persist to the adult stage

Holometabolous insects undergo a complete transformation of the body plan from the larval to the adult stage. In Drosophila, this transformation includes replacement of larval epidermal cells (LECs) by adult epidermal cells (AECs). AECs in Drosophila undergo a rapid and stereotyped aging program where they lose both cell membranes and nuclei. Whether LECs are capable of undergoing aging in a manner similar to AECs remains unknown. Here, we addressed this question in two ways. First, we looked for hallmarks of epidermal aging in larvae that have a greatly extended third instar and/or carry mutations that would alter the pace of epidermal aging at the adult stage. Such larvae, irrespective of genotype, did not show any of the signs of epidermal aging observed in the adult. Second, we developed a procedure to effect a heterochronic persistence of LECs into the adult epidermal sheet. Lineage tracing verified that presumptive LECs in the adult epidermis are not derived from imaginal epidermal histoblasts. LECs embedded within the adult epidermal sheet undergo clear signs of epidermal aging; they form multinucleate cells with each other and with the surrounding AECs. The incidence of adult cells with mixed AEC nuclei (small) and persistent LEC nuclei (large) increased with age. Our data reveal that epidermal aging in holometabolous Drosophila is a stage-specific phenomenon and that the capacity of LECs to respond to aging signals does exist.