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Morphological and histological examination of polyphenic wing formation in the pea aphid Acyrthosiphon pisum (Hemiptera, Hexapoda)

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Abstract

Aphids display divergent adult phenotypes, depending on environmental conditions experienced during their embyonic and nymphal stages in their complex life cycles. The plastic developmental mode is an extreme case of phenotypic plasticity, so-called “polyphenism”, in which discrete multiple phenotypes are produced based on a single genome. For example, winged and wingless adult females are derived from a single genotype. However, the developmental mechanisms producing these polyphenic traits according to the extrinsic stimuli, such as density conditions, still remain unknown. In this study, to analyze the developmental processes underlying the wing polyphenism, we extensively observed and compared wing development in the winged and wingless individuals in parthenogenetic generations of the aphid Acyrthosiphon pisum (Harris), using scanning electron microscopy and histological sectioning. At the first-instar stage, the wing primordia were observed both in the future winged (W) and wingless (WL) nymphs. Developmental differences can be seen from the second-instar stage, when wing primordia degenerate in the WL nymphs, while they develop and become more thickened in the W nymphs, suggesting that the developmental programs should be launched prior to this stage. Furthermore, during the third- to fifth-instar stages, wing buds and flight muscles were well developed in the W nymphs, while wing primordia completely disappeared in the WL ones. In addition, the observation on the detailed developmental process of wing primordia during the third-instar W nymphs showed that the wing buds become swollen especially at the basal part, even during the intermolt period. This was caused by the development of wing epithelia under the cuticle of this instar nymph. Actually on the surface of the cuticle of wing-bud bases, there were numerous furrows, which gradually expand during the intermolt period. The similar situation was also observed at the forth-instar nymphs, in which the wings are formed in the complicated manner inside the wing pads. Furthermore, the developmental process of flight muscles was also described in detail. These dynamic developmental differences between the wing morphs should be regulated under the gene expression cascades that switch according to environmental stimuli.

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Acknowledgments

We are grateful to S. Koshikawa, R. Cornette and T. Matsumoto for their valuable comments on the study and assistance in various experiments. The authors also thank D. Stern for his valuable comments and careful editing of the manuscript. Thanks are also due to T. Fukatsu and A. Nakabachi for providing aphid strains. This work was supported by Grants-in-Aid for Scientific Research (Nos. 15687001, 18047002 and 18370007) from the Ministry of Education, Culture, Sports, Science and Technology of Japan. This paper is dedicated to the Prof. Hajime Ishikawa of blessed memory.

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Authors and Affiliations

  1. Laboratory of Ecology and Genetics, Graduate School of Environmental Science, Hokkaido University, Sapporo, 060-0810, Japan

    Asano Ishikawa & Toru Miura

  2. Department of Biology, Graduate School of Arts and Sciences, University of Tokyo, 3-8-1 Komaba, Meguro, Tokyo, 153-8902, Japan

    Sakiko Hongo

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  1. Asano Ishikawa
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  2. Sakiko Hongo
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  3. Toru Miura
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Correspondence to Toru Miura.

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Ishikawa, A., Hongo, S. & Miura, T. Morphological and histological examination of polyphenic wing formation in the pea aphid Acyrthosiphon pisum (Hemiptera, Hexapoda). Zoomorphology 127, 121–133 (2008). https://doi.org/10.1007/s00435-008-0057-5

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