Abstract
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 language | English |
|---|---|
| Article number | 20190063 |
| Pages (from-to) | 1-8 |
| Number of pages | 8 |
| Journal | Philosophical Transactions of the Royal Society B: Biological Sciences |
| Volume | 374 |
| Issue number | 1783 |
| Early online date | 23 Aug 2019 |
| DOIs | |
| Publication status | Published - 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 journal › Article
}
TY - JOUR
T1 - Complete metamorphosis of insects
AU - Rolff, Jens
AU - Johnson, Paul
AU - Reynolds, Stuart
PY - 2019/10/1
Y1 - 2019/10/1
N2 - The majority of described hexapod species are holometabolous insects,undergoing an extreme form of metamorphosis with an intercalated pupalstage between the larva and adult, in which organs and tissues are extensively remodelled and in some cases completely rebuilt. Here, we reviewhow and why this developmental strategy has evolved. While there aremany theories explaining the evolution of metamorphosis, many of whichfit under the hypothesis of decoupling of life stages, there are few clear adaptive hypotheses on why complete metamorphosis evolved. We propose thatthe main adaptive benefit of complete metamorphosis is decouplingbetween growth and differentiation. This facilitates the exploitation ofephemeral resources and enhances the probability of the metamorphic transition escaping developmental size thresholds. The evolution of completemetamorphosis comes at the cost of exposure to predators, parasites andpathogens during pupal life and requires specific adaptations of theimmune system at this time. Moreover, metamorphosis poses a challengefor the maintenance of symbionts and the gut microbiota, although it mayalso offer the benefit of allowing an extensive change in microbiota betweenthe larval and adult stages. The regulation of metamorphosis by two mainplayers, ecdysone and juvenile hormone, and the related signalling cascadesare now relatively well understood. The mechanics of metamorphosis haverecently been studied in detail because of the advent of micro-CT andresearch into the role of cell death in remodelling tissues and organs. Wesupport the argument that the adult stage must necessarily have precededthe larval form of the insect. We do not resolve the still contentious questionof whether the larva of insects in general originated through the modification of existing preadult forms or through heterochrony as a modifiedembryonic stage (pronymph), nor whether the holometabolous pupa aroseas a modified hemimetabolous final stage larva.This article is part of the theme issue ‘The evolution of completemetamorphosis’.
AB - The majority of described hexapod species are holometabolous insects,undergoing an extreme form of metamorphosis with an intercalated pupalstage between the larva and adult, in which organs and tissues are extensively remodelled and in some cases completely rebuilt. Here, we reviewhow and why this developmental strategy has evolved. While there aremany theories explaining the evolution of metamorphosis, many of whichfit under the hypothesis of decoupling of life stages, there are few clear adaptive hypotheses on why complete metamorphosis evolved. We propose thatthe main adaptive benefit of complete metamorphosis is decouplingbetween growth and differentiation. This facilitates the exploitation ofephemeral resources and enhances the probability of the metamorphic transition escaping developmental size thresholds. The evolution of completemetamorphosis comes at the cost of exposure to predators, parasites andpathogens during pupal life and requires specific adaptations of theimmune system at this time. Moreover, metamorphosis poses a challengefor the maintenance of symbionts and the gut microbiota, although it mayalso offer the benefit of allowing an extensive change in microbiota betweenthe larval and adult stages. The regulation of metamorphosis by two mainplayers, ecdysone and juvenile hormone, and the related signalling cascadesare now relatively well understood. The mechanics of metamorphosis haverecently been studied in detail because of the advent of micro-CT andresearch into the role of cell death in remodelling tissues and organs. Wesupport the argument that the adult stage must necessarily have precededthe larval form of the insect. We do not resolve the still contentious questionof whether the larva of insects in general originated through the modification of existing preadult forms or through heterochrony as a modifiedembryonic stage (pronymph), nor whether the holometabolous pupa aroseas a modified hemimetabolous final stage larva.This article is part of the theme issue ‘The evolution of completemetamorphosis’.
KW - juvenile hormone, pupation, holometaboly, adaptation, insects
UR - http://www.scopus.com/inward/record.url?scp=85071454523&partnerID=8YFLogxK
U2 - 10.1098/rstb.2019.0063
DO - 10.1098/rstb.2019.0063
M3 - Article
VL - 374
SP - 1
EP - 8
JO - Philosophical Transactions of the Royal Society B: Biological Sciences
JF - Philosophical Transactions of the Royal Society B: Biological Sciences
SN - 0264-3839
IS - 1783
M1 - 20190063
ER -