![]() This shift proved remarkably beneficial: young and old insects were no longer competing for the same resources. Between 280 million and 300 million years ago, however, some insects began to mature a little differently-they hatched in forms that neither looked nor behaved like their adult versions. The earliest insects in Earth's history did not metamorphose they hatched from eggs, essentially as miniature adults. By combining evidence from the fossil record with studies on insect anatomy and development, biologists have established a plausible narrative about the origin of insect metamorphosis, which they continue to revise as new information surfaces. Metamorphosis is a truly bizarre process, but an explanation of its evolution does not require such unsubstantiated theories (for a critique of Williamson's hypothesis, see this study). Some scientists have proposed outlandish origin tales, such as Donald Williamson's idea that butterfly metamorphosis resulted from an ancient and accidental mating between two different species-one that wriggled along ground and one that flitted through the air. People have known since at least the time of ancient Egypt that worms and grubs develop into adult insects, but the evolution of insect metamorphosis remains a genuine biological mystery even today. Imprisoning someone for asserting what today qualifies as common knowledge might seem extreme, but metamorphosis-the process through which some animals abruptly transform their bodies after birth-has long inspired misunderstanding and mysticism. A few years later, Renous recounted his tale to Charles Darwin, who noted it in The Voyage of the Beagle. His claim? He could turn caterpillars into butterflies. This article is part of the theme issue 'The evolution of complete metamorphosis'.Īdaptation holometaboly insects juvenile hormone pupation.In the 1830s a German naturalist named Renous was arrested in San Fernando, Chile for heresy. 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.
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