Remodeling of the leg sensory system during metamorphosis of the hawkmoth, Manduca sexta.

Abstract

The adult legs of the hawkmoth Manduca sexta are supplied by a diverse array of sensory organs and associated neurons (Kent and Griffin [1990] Cell Tissue Res. 259:209-223) that differ from those in the larval legs. In the present study, a combination of nerve-tracing techniques [biocytin, 1,1;-dioctadecyl-3,3,3;, 3;-tetramethyl-indocarbocyanine perchlorate (DiI)], birth date labeling (5-bromodeoxyuridine), confocal microscopy, and electrophysiology were used to describe the remodeling of the prothoracic leg sensory system. Four primary sensory branches carry the axons of all of the sensory neurons in the larval leg. At the onset of metamorphosis, the imaginal leg epidermis develops underneath the larval cuticle and encircles the sensory neurons, thus separating them from their target-organs. Most of the larval neurons degenerate during the larval-to-pupal transition and are replaced by new-adult sensory neurons that are born and differentiate in the pupa. Six sensory neurons that supply hair sensilla in the larval leg, together with 13 femoral and tibial chordotonal organ neurons, persist into the developing adult leg to serve similar functions. Early in the pupal stage, electrical activity can be recorded from these neurons despite the absence of target sensory structures. During the differentiation of the adult sensory system, the axons of the new-adult sensory neurons contact and fasciculate with the axons of the persistent neurons. Thus, five of the primary sensory branches of the adult leg are built on the preexisting larval sensory trajectories. Two sensory branches, however, are established de novo by the axons of specific adult sensory neurons.