Rapid growth and the evolution of complete metamorphosis in insects

More than 50% of all animal species are insects that undergo complete metamorphosis. The key innovation of these holometabolous insects is a pupal stage between the larva and adult when most structures are completely rebuilt. Why this extreme lifestyle evolved is unclear. Here, we test the hypothesis that a trade-off between growth and differentiation explains the evolution of this novelty. Using a comparative approach, we find that holometabolous insects grow much faster than hemimetabolous insects. Using a theoretical model, we then show how holometaboly evolves under a growth-differentiation trade-off and identify conditions under which such temporal decoupling of growth and differentiation is favored. Our work supports the notion that the holometabolous life history evolved to remove developmental constraints on fast growth, primarily under high mortality.

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Publication Details

Journal
Proceedings of the National Academy of Sciences
Published
2024-09-09
DOI
https://doi.org/10.1073/pnas.2402980121
Citations
15
Primary Topic
Fossil Insects in Amber
Type
article
Field-Weighted Citation Impact
15.44

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article

Rapid growth and the evolution of complete metamorphosis in insects

Jens Rolff, Ulrich K. Steiner, Michael T. Monaghan, Christin Manthey et al.
15 citations
Proceedings of the National Academy of Sciences
Fossil Insects in Amber
15.44
article

Rapid growth and the evolution of complete metamorphosis in insects

Jens Rolff, Ulrich K. Steiner, Michael T. Monaghan, Christin Manthey, C. Jessica E. Metcalf
article en
15 citations

Abstract

More than 50% of all animal species are insects that undergo complete metamorphosis. The key innovation of these holometabolous insects is a pupal stage between the larva and adult when most structures are completely rebuilt. Why this extreme lifestyle evolved is unclear. Here, we test the hypothesis that a trade-off between growth and differentiation explains the evolution of this novelty. Using a comparative approach, we find that holometabolous insects grow much faster than hemimetabolous insects. Using a theoretical model, we then show how holometaboly evolves under a growth-differentiation trade-off and identify conditions under which such temporal decoupling of growth and differentiation is favored. Our work supports the notion that the holometabolous life history evolved to remove developmental constraints on fast growth, primarily under high mortality.

Proceedings of the National Academy of SciencesVol. 121(38)
Princeton University (US), Leibniz Institute of Freshwater Ecology and Inland Fisheries (DE), Institut de Biologia Evolutiva (ES), Freie Universität Berlin (DE)
Deutsche Forschungsgemeinschaft, Wissenschaftskolleg zu Berlin, Freie Universität Berlin
Openalex Percentile: Top 1%
Fossil Insects in Amber
15.44
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