The ecologist Henry Wilbur noted that many organisms have complex life cycles that include ‘an abrupt ontogenetic change in an individual's morphology, physiology and behaviour, usually associated with a change in habitat’. This article is part of the theme issue ‘The evolution of complete metamorphosis’.ġ. Introduction: what is complete metamorphosis? We do not resolve the still contentious question of whether the larva of insects in general originated through the modification of existing preadult forms or through heterochrony as a modified embryonic stage (pronymph), nor whether the holometabolous pupa arose as a modified hemimetabolous final stage larva.

We support the argument that the adult stage must necessarily have preceded the larval form of the insect. The mechanics of metamorphosis have recently been studied in detail because of the advent of micro-CT and research into the role of cell death in remodelling tissues and organs. The regulation of metamorphosis by two main players, ecdysone and juvenile hormone, and the related signalling cascades are now relatively well understood. Moreover, metamorphosis poses a challenge for the maintenance of symbionts and the gut microbiota, although it may also offer the benefit of allowing an extensive change in microbiota between the larval and adult stages. The evolution of complete metamorphosis comes at the cost of exposure to predators, parasites and pathogens during pupal life and requires specific adaptations of the immune system at this time. This facilitates the exploitation of ephemeral resources and enhances the probability of the metamorphic transition escaping developmental size thresholds. We propose that the main adaptive benefit of complete metamorphosis is decoupling between growth and differentiation. While there are many theories explaining the evolution of metamorphosis, many of which fit under the hypothesis of decoupling of life stages, there are few clear adaptive hypotheses on why complete metamorphosis evolved.

Here, we review how and why this developmental strategy has evolved. The majority of described hexapod species are holometabolous insects, undergoing an extreme form of metamorphosis with an intercalated pupal stage between the larva and adult, in which organs and tissues are extensively remodelled and in some cases completely rebuilt.

Stages of metamorphosis