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The origins of insect metamorphosis

Abstract

Insect metamorphosis is a fascinating and highly successful biological adaptation, but there is much uncertainty as to how it evolved. Ancestral insect species did not undergo metamorphosis and there are still some existing species that lack metamorphosis or undergo only partial metamorphosis. Based on endocrine studies and morphological comparisons of the development of insect species with and without metamorphosis, a novel hypothesis for the evolution of metamorphosis is proposed. Changes in the endocrinology of development are central to this hypothesis. The three stages of the ancestral insect species—pronymph, nymph and adult—are proposed to be equivalent to the larva, pupa and adult stages of insects with complete metamorphosis. This proposal has general implications for insect developmental biology.

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Figure 1: Comparison of the early immature stages of ametabolous, hemimetabolous and holometabolous insect species.
Figure 2: Endocrinology of embryonic and post-embryonic insect development.
Figure 3: The effects of the JH mimic pyriproxifen on Locusta embryos.
Figure 4: Relationship of the phylogeny of the Holometabola to the pattern of imaginal disc formation.
Figure 5: Possible steps in the transition from a hemimetabolous to a holometabolous life history and their relationship to timing of JH production (blue bar) and to growth directed towards the imaginal form (black triangles).

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Acknowledgements

We thank E. Ball for use of facilities at the Australian National University during the experimental phase of this study and for extensive comments on the manuscript. We also thank J. Edwards, J. Kingsolver, L. Nagy and D. Erezyilmaz for comments on drafts of this paper. This article is dedicated to the late G. B. Craig Jr, an inspirational force in the research and teaching of entomology.

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Correspondence to James W. Truman.

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Truman, J., Riddiford, L. The origins of insect metamorphosis. Nature 401, 447–452 (1999). https://doi.org/10.1038/46737

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