The evolution of insect metamorphosis: a developmental and endocrine view

Abstract

Developmental, genetic and endocrine data from diverse taxa provide insight into the evolution of insect metamorphosis. We equate the larva-pupa-adult of the Holometabola to the pronymph-nymph-adult of hemimetabolous insects. The hemimetabolous pronymph is a cryptic embryonic stage with unique endocrinology and behavioural modifications that probably served as preadaptations for the larva. It develops in the absence of juvenile hormone (JH) as embryonic primordia undergo patterning and morphogenesis, the processes that were arrested for the evolution of the larva. Embryonic JH then drives tissue differentiation and nymph formation. Experimental treatment of pronymphs with JH terminates patterning and induces differentiation, mimicking the processes that occurred during the evolution of the larva. Unpatterned portions of primordia persist in the larva, becoming imaginal discs that form pupal and adult structures. Key transcription factors are associated with the holometabolous life stages: Krüppel-homolog 1 (Kr-h1) in the larva, broad in the pupa and E93 in the adult. Kr-h1 mediates JH action and is found whenever JH acts, while the other two genes direct the formation of their corresponding stages. In hemimetabolous forms, the pronymph has low Broad expression, followed by Broad expression through the nymphal moults, then a switch to E93 to form the adult. This article is part of the theme issue 'The evolution of complete metamorphosis'.

Keywords: Broad; E93; Krüppel-homolog 1; juvenile hormone; pronymph.

Figure 1.

Life-history strategies in the insects. (a) Various life-history strategies characterized by silverfish, grasshoppers, sphinx moths and thrips, respectively. (b and c) The two major hypotheses for the evolution of the holometabolous stages from an unknown hemimetabolous ancestor. In (b), the larva arose from conversion of an embryonic stage (the pronymph) into the free-living, feeding larva and the nymphal stages were reduced to a non-feeding, transitional stage, the pupa [–4]. In (c), nymphs and larvae are considered equivalent and the last nymphal instar was modified into the transitional pupal stage [5,6]. (Online version in colour.)

Figure 2.

Comparison of embryonic and postembryonic development of a generalized hemimetabolous insect (cricket/grasshopper) with a holometabolous insect (moth). (a) Orthopteran development showing progressive patterning of the eye primordium and leg bud. Rows of ommatidia in the eye form as a wave of differentiation (arrows) moves anteriorly across embryonic primordium. CNS neuroblasts (NB) die late in embryogenesis after producing all of their neurons. The leg bud transforms into the leg by the recruitment of a sequence of proximal–distal patterning genes that determine the leg segments. These structures increase in size during nymphal life with little new additions except for ommatidia at the anterior margin of the eye. Based on [–20]. (b) Development in the moth embryo does not progress as far as that in the Orthoptera. Partially patterned systems serve as the basis of larval structures, but persisting embryonic centres (light orange) are carried into the larva and become the imaginal primordia that generate the adult structures. Based on [–,–24]. Hth, Homothorax; Exd, Extradenticle; Dll, Distal-less; Dac, Dachshund; Bab, Bric-a-brac. See text for more details.

Figure 3.

(a) Comparison of proliferation in early- and late-forming imaginal discs of M. sexta. The eye and wing imaginal primordia go through phases of nutrient-dependent proliferation (orange), morphogenetic proliferation (purple) and differentiative proliferation (green). Both primordia show nutrient-dependent growth in preterminal instars, but proliferation in the eye primordium is restricted to early in larval moults. Both primordia initiate morphogenetic growth early in the last instar and shift to differentiative divisions during the formation of the adult [24,33]. (b and c) Effects of br-dsRNA treatment on patterns of nymphal growth of O. fasciatus. (b) Growth of the leg (black) and wing pad (red) through the nymphal instars. The leg grows by a constant ratio throughout, but the wing pad shows enhanced growth during the last two nymphal moults. Suppression of Broad expression by injection of br-dsRNA in the 4th nymphal (N4) instar redirects the growth of the wing pad in line with the rest of the nymph (open symbol) (data from [34]). (c) Pictures of adults and their isolated forewings contrasting an animal going through a normal nymphal series (N#) to adult (A) with nymphs that were injected with br-dsRNA at the N4 or N3 instars (green). Subsequent instars repeat the features of the preceding instar and wing growth is suppressed (from [34]). (Online version in colour.)

Figure 4.

Comparison of the embryonic and postembryonic titres of ecdysteroids (black) and JH (blue) for (a) hemimetabolous insects, the grasshoppers L. migratoria (embryonic) and Schistocerca gregaria (postembryonic) and for (b) a holometabolous insect, M. sexta. The bars relate the presence of the respective cuticles to the hormone titers (cross-hatching represents pharate periods). Ecdysteroid titres are not available for Manduca embryos. Vertical dashed lines: times of ecdysis; Blasto, blastokinesis; DC, dorsal closure; E1, covered by the first embryonic cuticle; H, hatch. Ecdysteroid peaks: CP, commitment peak; PP, prepupal peak; PNP, pronymphal peak; NP, nymphal peak. Reprinted from [4]. (Online version in colour.)

Figure 5.

A generalized scheme shows in holometabolous insects how stage specification genes relate to each other, to the hormonal environment that orchestrates metamorphosis and to the cellular responses of the imaginal primordium and the general epidermis. Symbols that are greyed out are either absent or suppressed. See text for details. 20E, 20-hydroxyecdysone; Br, Broad; E93, Ecdysone-inducible protein 93F; JH, juvenile hormone; Kr-h1, Krüppel-homolog 1; MIF, metamorphosis initiation factor. Based on [24,57,59,61,63,65,66,69,70]. (Online version in colour.)

Figure 6.

Generalized diagram showing the relationship of Kr-h1, Broad and E93 expression to the various life stages of hemimetabolous, holometabolous and neometabolous insects. Based on [34,63,65,66,69,75,82,83]. See text for details. (Online version in colour.)