The innovation of the final moult and the origin of insect metamorphosis

Abstract

The three modes of insect postembryonic development are ametaboly, hemimetaboly and holometaboly, the latter being considered the only significant metamorphosis mode. However, the emergence of hemimetaboly, with the genuine innovation of the final moult, represents the origin of insect metamorphosis and a necessary step in the evolution of holometaboly. Hemimetaboly derives from ametaboly and might have appeared as a consequence of wing emergence in Pterygota, in the early Devonian. In extant insects, the final moult is mainly achieved through the degeneration of the prothoracic gland (PG), after the formation of the winged and reproductively competent adult stage. Metamorphosis, including the formation of the mature wings and the degeneration of the PG, is regulated by the MEKRE93 pathway, through which juvenile hormone precludes the adult morphogenesis by repressing the expression of transcription factor E93, which triggers this change. The MEKRE93 pathway appears conserved in extant metamorphosing insects, which suggest that this pathway was operative in the Pterygota last common ancestor. We propose that the final moult, and the consequent hemimetabolan metamorphosis, is a monophyletic innovation and that the role of E93 as a promoter of wing formation and the degeneration of the PG was mechanistically crucial for their emergence. This article is part of the theme issue 'The evolution of complete metamorphosis'.

Keywords: E93; evolution of insect metamorphosis; juvenile hormone; mekre93 pathway; origin of insect final moult; prothoracic gland degeneration.

Figure 1.

Cladogenesis of the main insect groups in a chronological context. The phylogenetic reconstruction is based on Misof et al. [11] and Wang et al. [12]. The main discrepancy between these two proposals is the situation of Paraneoptera, which is monophyletic for Wang et al. and polyphyletic for Misof et al. Divergence times are generally similar in both proposals. Those indicated here are based on the average values reported by Wang et al. [12]. Modified from [12]. (Online version in colour.)

Figure 2.

Palaeozoic and extant insects. (a) Selected developmental stages of Palaeozoic Mischoptera (Megasecoptera) species, from left to right, young nymph with articulated wings arched backwards (wing venation is still absent), older nymph with larger wings already showing wing venation, mature nymph or subadult with straighter wings and adult, with the wings practically perpendicular to the body axis. (b) Two Carboniferous roachoid nymphs, one in dorsal (left) and the other in ventral position, showing long wing pads. (c) Wing development in Palaeozoic and extant Ephemeroptera. Note the articulated and detached winglets in Palaeozoic mayflies and the winglets attached to the body in extant species. From [14].

Figure 3.

The MEKRE93 pathway exemplified by the cockroach Blattella germanica. (a) Juvenile hormone (JH) disrupts the homodimer Methoprene tolerant (Met)-Met, binds to Met, recruits the co-receptor Taiman (Tai), and the complex JH-Met + Tai induces the expression of Krüppel homolog 1 (Kr-h1), and Kr-h1 represses the expression of E93, which codes for the metamorphosis-triggering factor. (b) Early in the last (sixth) nymphal instar, the production of JH ceases, the expression of Kr-h1 decreases and that of E93 increases, thus bringing about the metamorphic moult.

Figure 4.

Depletion of E93 in the last nymphal instar of the cockroach Blattella germanica inhibits metamorphosis. The last nymphal instar (sixth) moults into a supernumerary (seventh) nymphal instar, with full nymphal features, including the absence of wings, instead moulting to a winged adult (left). After the imaginal moult, from the sixth nymphal instar, the prothoracic gland (PG) degenerates within the first days of adult life, but the E93-depleted, supernumerary (seventh) nymphal instar keeps an active PG and can moult again (right). Photos from Carolina G. Santos (left) and Orathai Kamsoi (right).

Figure 5.

The emergence of wings may have triggered the innovation of the last moult and the origin of (hemimetabolan) metamorphosis. One of the first innovations could have been the upregulation of E93 expression in mature nymphs. This could have contributed to wing maturation, prothoracic gland degeneration and adult commitment of epidermis. Another necessary requirement would be for JH to play an inhibitory role in metamorphosis, repressing E93, possibly through Kr-h1, as in extant insects. Refinements of this incipient MEKRE93 pathway would have adjusted the regulation of the genes involved, mainly Kr-h1 and E93, in different tissues and at the appropriate times. Differential solutions for ‘condensing’ juvenile and/or subadult stages in different lineages would have produced the life cycle diversity that we observe today in hemimetabolan species. The same Kr-h1–E93 axis could have regulated the tendency to attenuate the development of the wing pads in nymphal instars. (Online version in colour.)

Figure 6.

Phylogenetic analysis of E93 orthologues of Palaeoptera, Polyneoptera, Paraneoptera and Endopterygota species, as well as Thermobia domestica, as a representative of the ametabolan Zygentoma, and Catajapyx aquilonaris (Hexapoda, Diplura) as an hexapodan external group. Alignments were carried out with ClustalX [49] and phylogenetic reconstruction with RAxML [50], based on the maximum-likelihood principle, a JTT matrix, a gamma model of heterogeneity rate, and using empirical base frequencies and estimating proportions. The data were bootstrapped for 100 replicates. Bootstrap values are indicated in the subclass, superorder and order nodes. Scale bar indicates the number of substitutions per site. Complete species names and accession data of the respective sequences are detailed in the electronic supplementary material, table S1.