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Hypermetamorphosis in a leaf-miner allows insects to cope with a confined nutritional space

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Abstract

Hypermetamorphosis has been described in several Lepidoptera leaf-miner species (mostly Gracillariidae, Epipyropidae, and Phyllocnistidae) and can be defined as a strong modification of the larval morphology associated with a switch in its feeding mode. Evolution of this larval feeding strategy presumably influences nutritional resources that can be exploited and has strong consequences for plant morphology. The following study focuses on Phyllonorycter blancardella (Lepidoptera: Gracillariidae), a leaf-miner developing on Malus domestica. We characterize the morphology of larval mouthparts and the resulting morphological impact on leaf tissues. Our results show that first instars do not strongly affect the leaf anatomy and leave most plant cells intact, while later instars significantly disrupt leaf tissues. Additionally, young larvae are “fluid-feeders” and feed on plant cell fluids resulting from the progression of the larvae through the lower layer of the leaf spongy parenchyma. They occupy a feeding niche clearly distinct from later instars that are “tissue-feeders”. Hypermetamorphosis in P. blancardella most likely allows insects to cope with a confined nutritional space by partitioning the limited feeding resources, and may help leaf-miners to optimize their nutrition.

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Acknowledgments

We would like to thank Claude Lebos and Brigitte Arbeille from the Electronic Microscopy Platform of the University of Tours for their technical support. We also thank Ryan A. Richardson, Heidi Appel, Sylvain Pincebourde, Claudio R. Lazzari, Teresita C. Insausti and Jérôme Casas for helpful comments on the manuscript. We would like to thank the editor and two anonymous referees for useful comments and suggestions. This study has been supported by the ANR Grant No. ANR-05-JCJC-0203-01 and the Région Centre Project 201000047141 to David Giron. We thank Laurent Ardouin for full access to his orchard.

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Author notes

  1. Mélanie Body

    Present address: Division of Plant Sciences, 312 Christopher S. Bond Life Sciences Center, University of Missouri, 1201 Rollins Street, Columbia, MO, 65211, USA

  2. Vincent Burlat

    Present address: Université de Toulouse, UPS, UMR 5546, Laboratoire de Recherche en Sciences Végétales, BP 42617 Auzeville, 31326, Castanet-Tolosan, France

Authors and Affiliations

  1. Institut de Recherche sur la Biologie de l’Insecte, UMR CNRS 7261, Université François Rabelais, Parc Grandmont, 37200, Tours, France

    Mélanie Body & David Giron

  2. Biomolécules et Biotechnologies Végétales, EA 2106, Université François-Rabelais, 31 Avenue Monge, 37200, Tours, France

    Vincent Burlat

  3. CNRS, UMR 5546, BP 42617, 31326, Castanet-Tolosan, France

    Vincent Burlat

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  1. Mélanie Body
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Correspondence to Mélanie Body.

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Handling Editor: John F. Tooker.

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Body, M., Burlat, V. & Giron, D. Hypermetamorphosis in a leaf-miner allows insects to cope with a confined nutritional space. Arthropod-Plant Interactions 9, 75–84 (2015). https://doi.org/10.1007/s11829-014-9349-5

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