Complete metamorphosis of insects

Jens Rolff, Paul Johnson, Stuart Reynolds

Research output: Contribution to journalArticle

Abstract

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. Here, we review
how and why this developmental strategy has evolved. 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. We propose that
the main adaptive benefit of complete metamorphosis is decoupling
between growth and differentiation. This facilitates the exploitation of
ephemeral resources and enhances the probability of the metamorphic transition escaping developmental size thresholds. 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. 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 regulation of metamorphosis by two main
players, ecdysone and juvenile hormone, and the related signalling cascades
are now relatively well understood. 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. We
support the argument that the adult stage must necessarily have preceded
the larval form of the insect. 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.
This article is part of the theme issue ‘The evolution of complete
metamorphosis’.
Original languageEnglish
Article number20190063
Pages (from-to)1-8
Number of pages8
JournalPhilosophical Transactions of the Royal Society B: Biological Sciences
Volume374
Issue number1783
Early online date23 Aug 2019
DOIs
Publication statusPublished - 1 Oct 2019

Keywords

  • juvenile hormone, pupation, holometaboly, adaptation, insects

Cite this

Complete metamorphosis of insects. / Rolff, Jens; Johnson, Paul; Reynolds, Stuart.

In: Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 374, No. 1783, 20190063, 01.10.2019, p. 1-8.

Research output: Contribution to journalArticle

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