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A hemimetabolous wing development suggests the wing origin from lateral tergum of a wingless ancestor

Ohde, Takahiro Mito, Taro Niimi, Teruyuki 京都大学 DOI:10.1038/s41467-022-28624-x

2022

概要

The origin and evolution of the novel insect wing remain enigmatic after a century-long discussion. The mechanism of wing development in hemimetabolous insects, in which the first functional wings evolved, is key to understand where and how insect wings evolutionarily originate. This study explored the developmental origin and the postembryonic dramatic growth of wings in the cricket Gryllus bimaculatus. We find that the lateral tergal margin, which is homologous between apterygote and pterygote insects, comprises a growth organizer to expand the body wall to form adult wing blades in Gryllus. We also find that Wnt, Fat-Dachsous, and Hippo pathways are involved in the disproportional growth of Gryllus wings. These data provide insights into where and how insect wings originate. Wings evolved from the pre-existing lateral terga of a wingless insect ancestor, and the reactivation or redeployment of Wnt/Fat-Dachsous/Hippo-mediated feed-forward circuit might have expanded the lateral terga.

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Acknowledgements

We thank Drs. Tetsuya Bando and Sumihare Noji for their help in preliminary analysis

of Gryllus vg and sd function. We thank Dr. Toshiya Ando, and Dr. Takaaki Daimon and

his lab members for helpful discussion. We also thank Drs. Yuji Matsuoka, Takahito

Watanabe, Yohei Katoh, Taro Nakamura, Shinichi Morita, Hajime Ono, Miki Sugimoto,

and Mr. Takahisa Yamashita for technical supports. The computational resource for the

RNA-seq analysis was provided by NIG supercomputer system. This study was supported by JSPS KAKENHI (16K18825 and 19H02970 for T.O., 16H02596 for T.N.).

NATURE COMMUNICATIONS | (2022)13:979 | https://doi.org/10.1038/s41467-022-28624-x | www.nature.com/naturecommunications

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Author contributions

Reprints and permission information is available at http://www.nature.com/reprints

T.O.—conceptualization, methodology, formal analysis, investigation, writing—original

draft preparation, visualization, project administration, funding acquisition; T.M.—

methodology, validation, resources, writing—review and editing; T.N.—conceptualization, validation, resources, writing—review and editing, funding acquisition.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in

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Competing interests

The authors declare no competing interests.

Additional information

Supplementary information The online version contains supplementary material

available at https://doi.org/10.1038/s41467-022-28624-x.

Correspondence and requests for materials should be addressed to Takahiro Ohde.

Peer review information Nature Communications thanks Aleksandar Popadić and the

other anonymous reviewers for their contribution to the peer review of this work. Peer

reviewer reports are available.

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