Development of the adult leg epidermis in Manduca sexta: contribution of different larval cell populations

Abstract

During metamorphosis of the tobacco hornworm Manduca sexta, the simple thoracic legs of the larva are remodeled into the more complex adult legs. Most of the adult leg epidermis derives from the adult primordia, small sets of epidermal cells located in specific regions of the larval leg, which proliferate rapidly in the final larval instar. In contrast, the contribution of the epidermal cells outside the primordia is unknown. In this study we have determined their contribution to the adult leg by labeling them with 5-bromodeoxyuridine (BUdR) and following their fate. Although the labeled cells diminished drastically in number, small groups of these cells persisted into the midpupal stage suggesting that they do contribute to the adult leg epidermis. We also found that during the wandering stage the adult primordia went through active proliferation and very little cell death, while the cells outside the primordia went through extensive cell death accounting for the decrease in their number. Our results indicate that two distinct cell populations exist outside the adult primordia. Most cells belong to the first population, which is larval-specific and disappears through apoptosis early in metamorphosis. The second population consists of polymorphic cells that contribute to the larval, pupal and adult leg epidermis.

Larval legs of mulberry silkworm Bombyx mori are prototypes for the adult legs

“…Our results also validate the studies on leg development of Manduca sexta (Tanaka and Truman, 2005). They showed that the simple thoracic legs of larva are remodeled into adult multisegmented leg.…”

Positional Cloning of a Bombyx Wingless Locus flügellos (fl) Reveals a Crucial Role for fringe That Is Specific for Wing Morphogenesis

“…We are interested in understanding the difference in fng functions between Bombyx and Drosophila. It has been suggested that the developmental processes of organogenesis differ between the Lepidoptera and Drosophila (Kim 1959;Tanaka and Truman 2005;Allee et al 2006;Franco et al 2007). Drosophila imaginal organs develop from each imaginal disc in a concentric region.…”

“…However, in Bombyx and other Lepidoptera, most adult organs are derived from the immature epithelial region called the ''primordium,'' except for the wings, which develop from the wing imaginal discs. For example, Lepidoptera legs do not develop from imaginal discs but from the cylindrical epidermis of the caterpillar's legs (Kim 1959;Tanaka and Truman 2005). In the developing leg imaginal discs of Drosophila, Fng-mediated N signaling functions to establish segmentation and the promotion of leg growth (Rauskolb 2001).…”

Indirect development, transdifferentiation and the macroregulatory evolution of metazoans

“…This may have been the route for the origin of ciliated larvae in early metazoans ( figure 5a,b). This also seems to have been the general route for the evolution of indirect development in hemimetabolous insects ( figure 5c,d), which eventually resorted to extensive use of imaginal cells in the more derived long-germband clades (Svácha 1992;Tanaka & Truman 2005;Guha et al 2008;NakayamaIshimura et al 2009). Thus, the introduction of 'set-aside' imaginal discs seems to be a secondary shortcut to the original route of partial dedifferentiation and subsequent restoration of developmental potential, i.e.…”

“…In the silkworm, differentiated cells of the larval antennae contribute to the adult antennae, and imaginal discs derive from ectodermal differentiated cells (Svácha 1992). Similarly, differentiated cells of the larval legs contribute to the adult legs of the tobacco hornworm (Tanaka & Truman 2005). Therefore, differentiated cells maintain or regain developmental potency and then acquire new fates and proliferate during adult transformation.…”