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The homology of cephalic muscles and endoskeletal elements between Diplura and Ectognatha (Insecta)

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Abstract

Diplura (two-pronged bristletails) are key to our understanding of hexapod head evolution. A sister group relationship with Ectognatha (=Insecta), comprising bristletails, silverfish and winged insects, is advocated in most modern studies, however, homologization of head muscles and endoskeletal elements between Diplura and Ectognatha is still lacking. Here, we present the first homologization of a number of head muscles and endoskeletal structures between Diplura and Ectognatha. A homologization of these structures is possible if a range of species, both from Japygidae and Campodeidae, are studied in order to reconstruct the potential groundplan characteristics and account for inner anatomy variations within Diplura. Japygidae and Campodeidae show differences in the origin, insertion, and presence of mandibular and maxillary muscles as well as the shape of the maxillary cardo. Taking into account recent embryological studies on the formation of the endoskeleton in Protura, Collembola and Diplura, we furthermore reconstruct the potential evolution of the endoskeleton in early Hexapoda. The tentorium is a defining feature of dicondylic insects (including Archaeognatha) while anterior and posterior cephalic invaginations (the later tentorial pits of dicondylic insects) are groundplan features of Hexapoda. Additionally, we clarify the composition of the gnathal pouches (i.e. the type of entognathy) in Diplura and Collembola. The pouches in Diplura are posteriorly separated, similar to the state encountered in Collembola. This contrasts to former studies emphasizing the differences in the ellipuran and dipluran type of entognathy.

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Acknowledgments

Thomas Wesener kindly loaned specimens of Atlasjapyx cf. atlas; Nikolaus U. Szucsich determined the species and gave useful advice during the preparation of the mansucript and the review process. We additionally thank one anonymous reviewer. Peter T. Rühr, Makiko Fukui, Shigekazu Tomizuka, and Rolf G. Beutel are thanked for extremely useful discussion during the final preparation of this manuscript. Kaoru Sekiya collected Metriocampa sp., L. weberi, O. japonicus, and O. akiyamae; Alex Böhm collected C. aquilionaris. Cyrille d’Haese provided the majority of collembolans; Steven Yanoviak collected M. cundinamarcensis. Felix Beckmann, Fabian Wilde (both HZG / DESY), Marco Stampanoni, Peter Modregger and Rajmund Mokso (all PSI) as well as Kentaro Uesugi (SPring-8) provided excellent support at the synchrotron facilities. Bernhard Misof is thanked for his constant and unrelenting encouragement to AB.

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Authors and Affiliations

  1. Sugadaira Montane Research Center, University of Tsukuba, Sugadaira Kogen, Ueda, Nagano, 386-2204, Japan

    Alexander Blanke & Ryuichiro Machida

  2. Medical and Biological Engineering Research Group, School of Engineering, University of Hull, Hull, HU6 7RX, UK

    Alexander Blanke

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  1. Alexander Blanke
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  2. Ryuichiro Machida
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Correspondence to Alexander Blanke.

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Funding statement

Scanning was financed by DESY (proposal no. I-20090211, I-20100029 and I-20120065), PSI (20100137, 20110069 and 20140056) and SPring-8 (2014B1046) which is gratefully acknowledged. AB was financed by a post-doc fellowship of the Japanese Society for the Promotion of Science (JSPS ID: P14071), by a research fellowship of the Deutsche Forschungsgemeinschaft (DFG ID: BL 1355/1-1) and additionally supported by the joint research program of the DAAD and the University of Tsukuba (ID 57060275). RM received a grant-in-aid from the JSPS (Scientific Research C: 25440201).

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM_1

Muscle homologization between Diplura and dicondylic insects in MS-Excel format. Note that table one shows the muscle homologization while table two shows the origins and insertions of each muscle. (XLS 112 kb)

ESM_2

3D model of Atlasjapyx in .blend format (BLEND 58092 kb)

ESM_3

TIFF image stack of the reconstructed microCT dataset of Atlasjapyx in avi format for easy browsing through the stack. Mandible (red), maxillae (dark blue), hypopharyngeal fulturae (light blue), head capsule (purple). Note that the original TIFF image stack is 2560x2560 pixel with 2404 single images. The original dataset is available upon request due to the large size. (AVI 53983 kb)

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Blanke, A., Machida, R. The homology of cephalic muscles and endoskeletal elements between Diplura and Ectognatha (Insecta). Org Divers Evol 16, 241–257 (2016). https://doi.org/10.1007/s13127-015-0251-5

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