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Evolutionary History of Maternal Plant-Manipulation and Larval Feeding Behaviours in Attelabidae (Coleoptera; Curculionoidea) and Evolution of Plant-Basal Weevil Interaction

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Evolutionary Biology: Genome Evolution, Speciation, Coevolution and Origin of Life

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Abstract

Weevils are one of the dominant taxonomic groups in terrestrial ecosystem, diversifying to more than 60,000 described species. Although the most derived weevil group, Curculionidae, has adapted to and is utilising almost all parts of plant, basal groups show relatively limited larval feeding habits, such as pollen, seed, or fungus-infested wood feeders. Thus, it seems that ancestral larval infesting plant parts of weevils were restricted to N-rich, induced-defenseless, and temporal resources. Among the basal weevils, Attelabidae obtained such resources for their larvae by evolving unique maternal plant-manipulations: attelabid females manipulate specific young plant tissues of their host plants in a species-specific manner, e.g. cutting a shoot or a leaf, rolling a leaf, or constructing sophisticated wrapped leaf rolls, before and after oviposition presumably to secure the survivorship of eggs or larvae. Molecular phylogenetic analyses based on the nuclear 18S and 28S ribosomal DNA and the mitochondrial COI genes indicated that the maternal plant-cutting behaviour originated in a common ancestor of Attelabidae, but was subsequently lost in the several lineages. The monophyly was recovered for the subfamily Attelabinae with high support, but not for the subfamily Rhynchitinae. By employing maximum likelihood-based ancestral state reconstructions, the larval leaf-blade feeding was inferred to have evolved from the boring of cut shoots/petioles. Moreover, the maternal leaf-rolling behaviour might have originated independently in the Attelabinae, Byctiscini, and also in several Deporaini lineages. Since the sophisticated behaviour of Attelabinae, i.e. constructing wrapped leaf rolls, have originated only once and not been lost in the lineage, these complex and innovative behaviours may have contributed to the success of the lineage diversification.

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Acknowledgments

We wish to thank Dr. K Aoki, Dr. A Kawakita, Dr. H Nishi, Dr. R Goto and Y Kobayashi for supplying weevil samples. We also thank Dr. Y Kameda, and Dr. A Kawakita for their helpful advices regarding molecular techniques and the analysis of molecular phylogenies. We are grateful to Dr. H Kojima for identifying a curculionid weevil. We thank Dr. AA Legalov, Dr. A Riedel, Dr. Y Sawada and Dr. K Izawa for providing helpful and detailed information on weevil behaviours and lifestyles. This study was supported by JSPS Research Fellowships for Young Scientists.

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Authors and Affiliations

  1. Division of Ecology and Evolutionary Biology, Graduate School of Life Sciences, The University of Tohoku, 3−6 Aoba, Aramaki, Aoba, Sendai, Miyagi, 980-8578, Japan

    Chisato Kobayashi & Masakado Kawata

  2. Department of Botany, National Museum of Nature and Science, Amakubo 4−1−1, Tsukuba, Ibaraki, 305-0005, Japan

    Yudai Okuyama

  3. Graduate School of Human and Environmental Studies, Kyoto University, Yoshida-Nihonmatsu-cho, Sakyo, Kyoto, 606-8501, Japan

    Kazuhide Kawazoe & Makoto Kato

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  1. Chisato Kobayashi
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  2. Yudai Okuyama
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  3. Kazuhide Kawazoe
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  4. Masakado Kawata
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  5. Makoto Kato
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Correspondence to Chisato Kobayashi .

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  1. CNRS, Laboratoire Évolution Biologique et Modélisation, Université d'Aix-Marseille, Marseille, France

    Pierre Pontarotti

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Kobayashi, C., Okuyama, Y., Kawazoe, K., Kawata, M., Kato, M. (2014). Evolutionary History of Maternal Plant-Manipulation and Larval Feeding Behaviours in Attelabidae (Coleoptera; Curculionoidea) and Evolution of Plant-Basal Weevil Interaction. In: Pontarotti, P. (eds) Evolutionary Biology: Genome Evolution, Speciation, Coevolution and Origin of Life. Springer, Cham. https://doi.org/10.1007/978-3-319-07623-2_11

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