Origin and Evolution of Insect Metamorphosis

Abstract

Insect metamorphosis can be classified into three modalities: ametabolan (no changes), hemimetabolan (progressive changes) and holometabolan (dramatical changes at the end of the cycle). The metamorphic changes are mainly regulated by two hormones: the moulting hormone, which promotes the moults, and the juvenile hormone (JH), which represses the transformation into the adult. The action of these two hormones is mediated by a number of transcription factors, and the molecular mechanisms regulating the expression of these and of the corresponding target genes are finally refined by the action of micro ribonucleic acids. Among the different transcription factors involved, those of the Broad‐Complex group are especially interesting because they have a differential expression and JH dependency in holometabolans and hemimetabolans. Holometabolan metamorphosis probably evolved from hemimetabolan ancestors, although the mechanisms underlying such a transition are still obscure.

Key Concepts:

  • Insect metamorphosis can be classified into three modalities: ametabolan, hemimetabolan and holometabolan.

  • The main hormones involved in the regulation of insect metamorphosis are the moulting hormone and the juvenile hormone.

  • The molecular mechanisms underlying the action of the moulting hormone are reasonably well known, but those related to juvenile hormone are much less understood.

  • Broad‐Complex transcription factors are involved in the transduction of both, the moulting hormone and the juvenile hormone, but have a differential expression and juvenile hormone dependency in holometabolans and hemimetabolans.

  • Fossil record and phylogenetic reconstructions suggest that hemimetaboly evolved from ametabolan ancestors, whereas holometaboly derived from hemimetaboly.

  • Mechanisms underlying the evolutionary transitions from ametaboly to hemimetaboly and to holometaboly are still obscure and under debate.

Keywords: metamorphosis; insects; holometaboly; hemimetaboly; ametaboly; neometaboly; prometaboly; ecdysone; juvenile hormone; Broad‐Complex

Figure 1.

The main types of insect metamorphosis, ametabolan, hemimetabolan and holometabolan, and the subtypes of hemimetabolan, prometabolan and neometabolan. Quiescent stages are showed in a green square. Adult, reproductively competent stages are showed in a red square. In the ametabolans, the red square is open because the adult continues moulting. Modified from Sehnal et al.. Published with permission from Elsevier.

Figure 2.

Hexapodan phylogeny, with indication of the types of metamorphosis in the different taxa. The phylogenetic reconstruction is based on Wheeler et al., Grimaldi and Engel and Kjer et al..

Figure 3.

(a) An experiment of parabiosis with the kissing bug, Rhodnius prolixus. Typically, VB Wigglesworth connected two specimens at different developmental stages and one mediated the fate of the other, thanks to the factors transported by the shared haemolymph. With these experiments, Wigglesworth demonstrated the existence of moulting and juvenile hormones. Photograph courtesy of the late Vincent B. Wigglesworth. (b) Structure of the main metamorphosis hormones in insects: ecdysone is the precursor of 20‐hydroxyecdysone, the most common moulting hormone in insects; juvenile hormone III is the most common JH in insects.

Figure 4.

Diagram of the hormone titres and expression of Broad‐Complex (BR‐C) transcription factors in the last developmental instars in a hemimetabolan (the German cockroach, Blattella germanica) and a holometabolan (the tobacco hornworm, Manduca sexta). Hormone titres of B. germanica are from Romaña et al. and Treiblmayr et al., and BR‐C data are from Belles X and Huang J‐H (unpublished). Hormone titres and BR‐C data of M. sexta are from Riddiford et al.. HCS, head capsule slippage.

Figure 5.

Successive stages in the biological cycle of the Ripiphorid beetle Rhipidius quadriceps, which is endoparasitic of cockroaches. (a) Triungulin larva, legged and very mobile (it searches the host and penetrates into it); (b–c) second larval type in different states of growth (which lives within the host); (d) third larval type (which also lives within the host); (e) fourth larval type (which leaves the host and pupates outside); (f) male pupae; (g) female pupae; (h) adult male and (i) adult female. Hypermetamorphic species like R. quadriceps can be key subjects to study the regulation and the evolution of insect metamorphosis. Drawings courtesy of Claude Besuchet.

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Belles, Xavier(Mar 2011) Origin and Evolution of Insect Metamorphosis. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0022854]