Chapter 12 - The evolution of metamorphosis

Abstract

Hemimetaboly gave rise to holometaboly, whose main advantage is the capacity of the larvae to exploit new resources. The pupal stage, consubstantial with the emergence of holometaboly, serves as a bridge between the divergent larva and the adult. Two alternative theories explain the origin of holometaboly. One is the pronymph theory, which contends that holometabolan embryogenesis is “arrested” at the pronymph stage and resumed in the pupa. Thus, the hemimetabolan pronymph would be homologous to the holometabolan larvae, while the hemimetabolan nymphs would be homologous to the pupa. Alternatively, the theory of direct homology between stages proposes that the nymphal program is not “arrested” in holometabolan embryogenesis but continues with the larval program. Thus, the nymphs would be homologous to the larvae, the pupa being only a modified las instar nymph. Observations on the embryo suggest that both hemimetabolans and holometabolans follow an equivalent development, whereas experiments on the embryonic functions of juvenile hormone (JH) suggest that they are less important than previously thought. The gene Broad-complex (BR-C) is especially interesting. In hemimetabolans, BR-C is expressed through the nymphal period enhanced by JH and promotes the development of wings. In holometabolans, BR-C is repressed by JH during larval instars, so it is expressed at the end of the last larval instar, after a decline of JH, and triggers the formation of the pupa. In the last nymphal instar and in the pupa, JH production falls, the expression of the JH-dependent gene Kr-h1 also falls, which de-represses the expression of E93, whose gene product triggers the adult morphogenesis, a regulatory axis known as the MEKRE93 pathway. Data available rather support the theory of direct homology between stages. In this frame, a shift in JH action on BR-C expression, from stimulatory to inhibitory, might have been a key mechanism allowing the transition from hemimetaboly to holometaboly. It would have triggered at the same time the qualitative transformation of the nymph into a larva and the emergence of the pupal stage.